| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
3Department of Plant Sciences, Montana State University, Bozeman, Montana 59717 USA; 4Tropical Biology Group, Royal Botanic Garden Edinburgh, 20a Inverleith Row, Edinburgh EH3 5LR, UK; 5Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK; 6Department of Biological Sciences, University of Dundee, Dundee DD1 4HN, UK; and 7Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão No. 915, Gavea 22.460 Rio de Janeiro—RJ, Brazil
Received for publication January 11, 2000. Accepted for publication June 2, 2000.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITEDAPPENDIXAPPENDIX |
|---|
Key Words: aeschynomenoid nodule • dalbergioid legumes • Fabaceae • papilionoid legumes • root nodule
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITEDAPPENDIXAPPENDIX |
|---|
|
). Three subtribes were recognized: Pterocarpeae with samaroid pods, Lonchocarpeae marked by pods having at most small marginal wings, and Geoffroyeae having drupaceous fruits. Polhill (1971, 1981d, 1994)
revised this classification by combining morphological evidence with that of seed chemistry and wood anatomy. This new Dalbergieae included 19 tropical woody genera mainly from Bentham's Pterocarpeae and Geoffroyeae. Lonchocarpinae were relegated to a closer relationship with other legumes that accumulated nonprotein amino acids in seed (e.g., Evans, Fellows, and Bell, 1985
). The revised Dalbergieae were diagnosed by supposedly plesiomorphic flower morphologies (i.e., free keel petals, staminal filaments partly fused and without basal fenestrae), pods with specialized seed chambers, and seeds that accumulated alkaloids or other than nonprotein amino acids. Geesink (1981, 1984)
accepted Polhill's circumscription with slight modification, whereas Sousa and de Sousa (1981)
proposed a classification similar to Bentham's because Dalbergieae (sensu Polhill, 1981d
) supposedly shared a determinate inflorescence with the Lonchocarpinae.
The Aeschynomeneae (Rudd, 1981a
) are one of five tribes traditionally characterized by lomented pods (Polhill, 1981a
). Although some Aeschynomeneae lack such pods (e.g., Arachis, Ormocarpopsis, Diphysa spp., Ormocarpum spp., Pictetia spp.), none of the members of this tribe have ever been confused or classified with the genera of Dalbergieae. Adesmieae (Polhill, 1981f
) have a notable history independent of the other dalbergioid legumes. This is because this tribe combines a presumed plesiomorphic trait, free staminal filaments, with a supposedly very derived one, lomented pods. This combination has suggested either a taxonomically isolated position or a relationship with other papilionoids also with free stamens (e.g., Burkart, 1952
). Bryinae, with lomented pods, possess other traits confirming its placement in the tribe Desmodieae (e.g., explosive secondary pollen presentation; Ohashi, Polhill, and Schubert, 1981
). However, Bryinae have seeds that do not accumulate nonprotein amino acids and lack a structural mutation in the chloroplast rpl2 locus (Bailey et al., 1997
). Both are atypical of the rest of Desmodieae.
In spite of a taxonomic history of Dalbergieae that has been separate from those of Aeschynomeneae, Adesmieae, and Bryinae, we present evidence that they collectively form a monophyletic group. The focus on these putatively disparate taxa was motivated by the taxonomic distribution of the distinctive aeschynomenoid root nodule (Corby, 1981
; Faria et al., 1994
) and four cladistic analyses: three involving nonmolecular data (Lavin, 1987
; Chappill, 1995
; Beyra-M. and Lavin, 1999
), and one with rbcL sequence data (Doyle et al., 1997
). We have expanded on these previous analyses by sampling exhaustively to reveal the exact constituents of the dalbergioid clade and enumerate the nonmolecular characters that have been used in the conventional tribal classification of these legumes. As such, we demonstrate where molecular and nonmolecular data are taxonomically concordant. We also show that many traditionally important taxonomic characters in this group are more homoplasious than previously considered. Because taxon sampling has focused on just the putative members of the dalbergioid clade, a point to be briefly addressed here but more thoroughly developed elsewhere is the higher level relationships of this newly recognized clade (Hu et al., 2000
; Pennington et al., in press
; M. Wojciechowski et al., unpublished data).
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITEDAPPENDIXAPPENDIX |
|---|
and Delgado-Salinas et al. (1999)
. Primers for matK and flanking trnK intron sequences are described in Lavin et al. (2000)
. Primers for the trnL intron are described by Taberlet et al. (1991)
. DNA sequencing was performed on an automated sequencer at the Iowa State University DNA Sequencing Facility (Ames, Iowa, USA) and Davis Sequencing (Davis, California, USA).
DNA sequences were aligned manually with Se-Al (Rambaut, 1996
). Bias introduced by the manual alignment was evaluated with a sensitivity analysis (cf. Whiting et al., 1997
; Beyra-M. and Lavin, 1999
; Delgado-Salinas et al., 1999
). Alignment-variable regions were variably aligned or excluded, a step matrix (cf. Cunningham, 1997
) was invoked or not, and gaps were treated as missing data, a fifth state, or as separate characters. Each of the different sensitivity analyses were subjected to the same heuristic search options. Missing data included 12.9% of the matK/trnK data set, 5.4% of the trnL data set, 1.5% of the ITS/5.8S data set, and 7.6% of the nonmolecular data set.
Maximum parsimony analyses were performed with PAUP* (Swofford, 2000
). Heuristic search options included 100 random-addition replicates, tree- bisection-reconnection branch swapping, and steepest descent. A maximum of 10 000 trees was allowed to accumulate, which is sufficient to capture all topological variation (cf. Sanderson and Doyle, 1993
). Clade stability tests involved bootstrap resampling (Felsenstein, 1985
; Sanderson, 1995
), where each of the 10 000 bootstrap replicates was subjected to heuristic search options that included one random-addition sequence per replicate, swapping with tree-bisection-reconnection, and invoking neither steepest descent nor mulpars.
Taxon sampling
Sampling of molecular and nonmolecular data was as exhaustive as possible at the generic level in order to determine membership in the dalbergioid clade, as well as the principal phylogenetic structure within this clade. Molecular and nonmolecular data were obtained for at least one species from every genus ever placed in the Dalbergieae (Burkart, 1952
; Polhill, 1981d
), Aeschynomeneae (Rudd, 1981a
), Adesmieae (Polhill, 1981f
), or Bryinae (Ohashi, Polhill, and Schubert, 1981
). The only exception is the presumably extinct genus Peltiera (Labat and Du Puy, 1997
), where no successful PCR amplifications were obtained from the few available DNAs. In addition to the advantages of being able to detail the taxonomic implications, exhaustive sampling for molecular data increases the probability of subdividing long branches (e.g., Hillis, 1998
).
Our original intent was to sample the same DNA accessions for each of the data sets. This proved impossible for DNA sequences because of inconsistencies in DNA quality and quantity and PCR amplification. We consequently had to resort to multiple methods of sampling. The DNA sequence data were sampled using the exemplar approach. Multiple species per terminal taxon were sampled where possible (Appendix A). Because nonmolecular data are generally open to visual inspection across all species of a particular terminal taxon, the "democratic" method of sampling (Bininda-Emonds, Bryant, and Russell, 1998
) was used for nonmolecular data. In this approach, we included all possible character states represented by any one terminal, which was usually a traditionally recognized genus (i.e., multistate terminal taxa were coded). The reasoning is that in the evaluation of traditionally important taxonomic characters, the degree of polymorphisms within terminals should be explicitly enumerated. For those few terminals in which species-level phylogenetic analysis has been completed (e.g., Andira and Pictetia), we employed the ancestral method of sampling nonmolecular data (Bininda-Emonds, Bryant, and Russell, 1998
). The justification for ultimately combining data that have been sampled differently is that a combined analysis should still allow us to best estimate where the traditionally important taxonomic characters lie on the continuum from strongly phylogenetically constrained to maximally homoplasious.
The genera Bergeronia, Dalbergiella, Lonchocarpus, and Muellera have been placed in the tribe Dalbergieae (e.g., Burkart, 1952
; Geesink, 1981
) and Pongamiopsis has been synonymized with the genus Aeschynomene (Hutchinson, 1964
). However, they were not included in this analysis because other phylogenetic analyses (Lavin et al., 1998
; Hu et al., 2000
) have shown these genera to be closely related to Millettia and relatives, all of which accumulate nonprotein amino acids in seed. Similarly, Poecilanthe and Cyclolobium should be allied with more basal Papilionoideae that accumulate alkaloids in seed (Greinwald et al., 1995
; Lavin et al., 1998
; Hu et al., 2000
). This is the reason that Poecilanthe is retained as a designated outgroup.
Outgroups were sampled extensively as part of large-scale molecular phylogenetic studies of the subfamily Papilionoideae (Hu et al., 2000
; Pennington et al., in press
; M. Wojciechowski et al., unpublished data). Sampling outgroups was guided by phylogenetic studies involving nonmolecular data (e.g., Chappill, 1995
; Herendeen, 1995
; Beyra-M. and Lavin, 1999
). For example, all outgroups chosen have leaves with punctate glands, a trait common to dalbergioids. In the end, the outgroups retained in this analysis included Acosmium and Myrospermum (tribe Sophoreae; Polhill, 1981b
), Dipteryx and Pterodon (Dipterygeae; Polhill, 1981c
), Poecilanthe (variously classified; see Lavin and Sousa, 1995
), and Apoplanesia, Amorpha, Eysenhardtia, and Marina (tribe Amorpheae; Barneby, 1977
; Polhill, 1981e
). This sampling was considered sufficient to demonstrate membership in the dalbergioid clade. The findings reported here did not change with a more extensive sampling of outgroups.
Sampling for the molecular data was re-evaluated as aligned DNA sequences accumulated. It became obvious that the matK/trnK sequences were by far the most informative at higher taxonomic levels, as seen in increased resolution in the strict consensus and higher bootstrap values. The primary effort then changed to sample as exhaustively as possible matK/trnK sequences and, secondarily, the ITS/5.8S and trnL intron sequences. Thus, the data analysis of this study centers on the matK/trnK data set. Sampling of ITS/5.8S sequences was guided by species level analyses of certain dalbergioid genera (e.g., Beyra-M. and Lavin, 1999
; Lavin et al., 2000
). Sampling of the trnL intron data was guided by a phylogenetic analysis of putatively basal Papilionoideae (Pennington et al., in press
). Unevenness in sampling was exacerbated by inconsistencies in PCR amplifications (mentioned above). A combined molecular analysis was not attempted because unevenness in sampling would result in a combined data set not exhaustively sampled at the genus level. Thus, consensus among the data sets was evaluated by congruence of the major clades resolved with high bootstrap values (cf. Huelsenbeck, Bull, and Cunningham, 1996
).
Nonmolecular character analysis
A nonmolecular data set was developed from that in Beyra-M. and Lavin (1999)
and is presented in Appendix B. Characters that have been considered traditionally important in the taxonomy of Dalbergieae, Aeschynomeneae, Adesmieae, and Bryinae (e.g., Burkart, 1952
; Ohashi, Polhill, and Schubert, 1981
; Polhill, 1981d
; Rudd, 1981a
; Sousa and de Sousa, 1981
) were targeted for analysis. As discussed above, multistate taxa were coded as polymorphic (cf. Weins, 1995
; Weins and Servedio, 1997
), in spite of the recommendation of Nixon and Davis (1991)
. Although this can underestimate the degree of homoplasy (see individual character discussions in Appendix B), splitting polymorphic terminals into two or more monomorphic ones does not change our findings (e.g., as evaluated in the fashion of a sensitivity analysis). This is because the focus is strictly at wide-scale relationships of groups of genera, and the potentially problematic polymorphisms are at a different level, within genera. Polymorphisms are discussed in the presentation of characters or ingroup terminal taxa (Appendices B and C). Inapplicable character states in certain terminals (e.g., leaf traits of Ramorinoa, a genus that doesn't produce leaves) were variously treated as a missing state, an uncertain state, or an extra state (as in a sensitivity analysis). The nonmolecular data were gathered primarily from field observations or herbarium specimens. Literature reports were usually verified by observations of the plants.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITEDAPPENDIXAPPENDIX |
|---|
|
|
|
Because of the poorly resolved relationships obtained from analysis of the nonmolecular data set, it was combined with the matK/trnK data set in order to explore the evolution of the traditionally important taxonomic characters. Integration with just the matK/trnK is justified by how well this data set can resolve relationships (discussed in MATERIALS AND METHODS) and because of noncompatibility of molecular data sets with respect to sampling. Parsimony analysis of the 1319 informative characters of the combined matK/trnK and nonmolecular data set (95 taxa by 3021 characters) produced 2340 trees with a minimal length of 4664, each with a consistency index of 0.551 and a retention index of 0.821. The resulting relationships are essentially those described previously for the analysis of just the matK/trnK data set (Fig. 5).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITEDAPPENDIXAPPENDIX |
|---|
1100 species of trees, shrubs, and perennial to annual herbs. Included are economically important hardwoods (e.g., Dalbergia and Pterocarpus spp.), forage legumes (Stylosanthes spp.), and crops (e.g., Arachis spp.). Like most pantropical legume taxa, the dalbergioids are concentrated in the neotropics and subSaharan Africa. Although the position of the dalbergioid clade within the Fabaceae is not fully developed here, its sister group is the tribe Amorpheae, which contains eight New World genera confined mostly to warm temperate and tropical North America. What is generally certain of higher level relationships is that the dalbergioids are distantly related to papilionoids that accumulate nonprotein amino acids in seed. This most notably includes Lonchocarpus, Derris, Millettia, and Hologalegina (e.g., tribes Robinieae, Galegeae, etc.; Wojciechowski, Sanderson, and Hu, 1999
), which at times have been taxonomically confused with various elements now included in the dalbergioid clade.
Implications for traditional classifications
The classification of certain genera into tribes and subtribes of Papilionoideae (e.g., Rudd, 1981a
; Ohashi, Polhill, and Schubert, 1981
; Ohashi, 1999
; Polhill, 1981a, d
) needs to be greatly modified in light of the evidence presented here. The genera Brya and Cranocarpus (subtribe Bryinae of tribe Desmodieae) share many unusual synapomorphies, such as periporate pollen and glochidiate trichomes, that have served to obscure higher level relationships. The explosive pollen presentation mechanism that Brya shares in common with Desmodieae is shown to have evolved independently. So have the lomented pods that Brya and Cranocarpus share with Desmodieae.
Four of the five subtribes of Aeschynomeneae are either monotypic (e.g., Discolobiinae) or are polyphyletic. Aeschynomeneae subtribe Ormocarpinae includes three different elements: Diphysa, Ormocarpum, Ormocarpopsis (and Peltiera), and Pictetia form one lineage in the Dalbergia clade, Fiebrigiella is in the Pterocarpus clade, and Chaetocalyx and Nissolia are part of the Adesmia clade. The pod valves with distinctive parallel venation that previously allied all of these genera now are considered to have evolved on three separate occasions. Indeed, this derived pod trait is homologous among Fiebrigiella, Chapmannia, Arachis, and Stylosanthes.
Aeschynomeneae subtribe Poiretiinae includes two different elements. Amicia, Poiretia, and Zornia form a monophyletic group within the Adesmia clade, and Weberbauerella is phylogenetically isolated within the Dalbergia clade. The marked pustular glands of Weberbauerella are no longer considered homologous to those of Amicia, Poiretia, and Zornia. In the recent classification of Japanese legumes (Ohashi, 1999
), Poiretia and Zornia are classified as the sole members of the tribe Poiretieae, a taxonomy that finds no support in this analysis.
Aeschynomeneae subtribe Aeschynomeninae includes eight genera (Aeschynomene, Cyclocarpa, Soemmeringia, Kotschya, Smithia, Humularia, Bryaspis, and Geissaspis) that form a very well-supported monophyletic group. A nonmolecular character supporting this relationship is the medifixed stipule, although it is not universal in this clade and has evolved independently in Zornia. An extrapolation from our small sample, however, suggests that species of Aeschynomene having basifixed stipules (e.g., A. fascicularis and A. purpusii) are more closely related to Machaerium and Dalbergia than they are to the species of Aeschynomene with medifixed stipules. Thus, the subtribe Aeschynomeninae includes two disparate elements.
Only Aeschynomeneae subtribe Stylosanthinae, with Arachis, Stylosanthes, and Chapmannia (and the segregates Pachecoa and Arthrocarpum), has been long recognized as a distinct taxonomic group and is also revealed as monophyletic in this analysis. The well-known nonmolecular character supporting the monophyly of this clade is a sessile papilionoid flower with a long hypanthium. However, these three genera are very closely related to Fiebrigiella and Fissicalyx and together all of these genera are set apart from other members of the Pterocarpus clade by large genetic distances. Notably, nonmolecular characters do not support most of the relationships in this clade that are so well supported by independent molecular data. For example, there are no known nonmolecular data that support the monophyly of the genus Chapmannia (Thulin, 2000
) or the relationship of Fissicalyx and Fiebrigiella.
The tribe Dalbergieae also is not monophyletic. Excluded from the dalbergioid clade are Andira, with 30 species largely confined to the neotropics and with one species distributed in the neotropics and tropical Africa (Lima, 1990
; Pennington, 1996
; Pennington, Aymard, and Cuello, 1997
), Hymenolobium with 10–15 species in tropical South America and one species in Central America (Polhill, 1981d
; Lima, 1982a, 1990
), Vatairea with seven species from Mexico to Brazil (Lima, 1982b, 1990
), and Vataireopsis with three species in Brazil and the Guianas (Polhill, 1981d
; Lima, 1990
). The distinction of these four genera from others traditionally included in the tribe Dalbergieae has been noted with wood anatomy (Baretta-Kuipers, 1981
) and estimates of overall similarity (Lima, 1990
). For example, the wood of Andira, Hymenolobium, Vatairea, and Vataireopsis lacks the storied structure and uniseriate rays that are characteristic of dalbergioid wood and is generally of less commercial value.
The remaining genera of the tribe Dalbergieae belong to either the Dalbergia or Pterocarpus clades. Only Dalbergia and Machaerium are part of the Dalbergia clade, where they are most closely related to Aeschynomene species that have basifixed stipules. The rest of the genera previously classified in the tribe Dalbergieae form the bulk of the Pterocarpus clade along with some genera previously classified in the tribe Aeschynomeneae (e.g., Fiebrigiella, Chapmannia, Arachis, Stylosanthes, and Discolobium) and subtribe Bryinae of Desmodieae.
The genera of Dipterygeae (Taralea, Dipteryx, and Pterodon; Polhill, 1981c
) are not part of the dalbergioid clade. Burkart (1952)
originally included Dipteryx (then Coumarouna) in the tribe Dalbergieae, and a phylogenetic analysis of nonmolecular data by Beyra-M. and Lavin (1999)
suggested Dipterygeae was part of the dalbergioid clade. Even the combination of paripinnate leaves bearing glandular punctae is known only from Dipterygeae and the dalbergioid legumes. However, this analysis strongly suggests that the punctate glands are plesiomorphic because they are found in all genera included in this analysis. Paripinnate leaves evolved independently among Dipterygeae and various elements in the dalbergioid clade.
Phylogenetic information among the various nonmolecular characters
While the matK/trnK phylogeny was not greatly influenced by the addition of the 55 nonmolecular characters (compare Figs. 2 and 5), there is some phylogenetic information in the nonmolecular characters, as evinced by high retention indices (Table 1). The consistency (CI) and retention (RI) indices for each of the 55 nonmolecular characters (Appendix B) in the combined analysis were compared to the same values obtained when each of the nonmolecular characters was mapped onto the matK/trnK phylogeny. In the combined analysis, the average CI and RI were 0.427 and 0.672, respectively. When mapped onto the matK/trnK trees, the average CI and RI were 0.390 and 0.627, respectively. Regardless of the small but significant differences (for RI, two-tailed t test, t = 2.94, P = 0.005, df = 52), no character had a higher consistency or retention index when mapped onto the matK/trnK phylogeny as when combined with the matK/trnK sequence data during parsimony analysis. This suggests that mapping a few selected nonmolecular characters onto a molecular phylogeny may involve a bias of excess levels of homoplasy.
|
for vascular plants, weakens the suggestion of Tucker and Douglas (1994)
that floral characters necessarily provide the best taxonomic information in Leguminosae. These findings also weaken the implication that pod morphology is prone to higher rates of convergent evolution than other types of characters (e.g., Geesink, 1984
; Hu et al., 2000
).
Conventional taxonomic evidence
Some traditionally important taxonomic characters are determined in this analysis to be more homoplasious than previously considered. This is especially true of the character states of growth habit, staminal fusion, and pod segmentation. Herbaceous and woody relatives generally are separated into different taxonomic groups when a temperate vs. tropical distinction correlates with habit (Judd, Sanders, and Donoghue, 1994
). This is especially true of papilionoid legumes where tribes have been categorized by habit (e.g., temperate herbaceous vs. tropical woody tribal division in Polhill, 1981a, 1994
). An herbaceous habit (number 1 in Appendix B) has evolved at least three times in monomorphic condition but more times than this in polymorphic condition (Table 1). The Adesmia clade contains mostly herbaceous species, although some species of Adesmia and Poiretia are shrubs. That an herbaceous growth form maps as the ancestral state in the Adesmia clade stands in contrast to the conventional wisdom that woody taxa form basal clades in tropical Papilionoideae (e.g., Polhill, 1981a
; Tucker and Douglas, 1994
).
Genera containing both woody and herbaceous species also occur in the clade containing Aeschynomene sect. Aeschynomene, Kotschya, Humularia, and Geissaspis. The same is true for the clade including Fiebrigiella, Chapmannia, Stylosanthes, and Arachis. Fissicalyx and some species of Chapmannia are woody in a clade dominated by herbaceous to subshrubby species. Representing yet two other clades, species of Machaerium, Dalbergia, Brya, and Cranocarpus vary from trees or shrubs to weak subshrubs. Clearly, there is no evidence from this analysis that the ability to produce a strongly woody growth habit is a good indicator of relationship.
The staminal character number 26 (Appendix B) includes five states that provide an average length of 15.0 to the most parsimonious trees. The consistency index of 0.267 and the retention index of 0.633 demonstrate that this character is homoplasious. Even state zero, free staminal filaments, added a length of two because this state occurs ancestrally in some of the outgroup genera and represents a reversion in the genus Adesmia. That a legume group with free stamens can evolve this condition secondarily from a fused condition (e.g., 9 + 1 diadelphous) is not surprising. Four species of Pictetia have nearly free staminal filaments in a clade otherwise represented by species with fused filaments (Beyra-M. and Lavin, 1999
). Also, Käss and Wink (1995, 1997)
have implicitly shown in an unrelated papilionoid group that the evolution of staminal morphology does not necessarily involve a unique transformation from free filaments into the fused condition. Perhaps related to this issue, Klitgaard (1999a)
showed that order of initiation and loss of stamens are more variable among the dalbergioids than previously appreciated. No doubt, the a priori view that free staminal filaments represent necessarily a plesiomorphic condition among papilionoid legumes will have to be abandoned.
All papilionoid legumes with lomented pods were at one time classified together, although more recently five tribes (Adesmieae, Aeschynomeneae, Coronilleae, Desmodieae, and Hedysareae) were thought to have gained this pod type independently (Polhill, 1981a
). We scored three states pertaining to articulation of pod segments (number 31 in Appendix B), which added an average length of 9.0 to the most parsimonious trees. The consistency index of 0.250 and a retention index of 0.825 suggest that, although homoplasious, this character provided phylogenetic resolution towards the tips of the tree. The Adesmia clade is uniform for lomented pods, but the Dalbergia and Pterocarpus clades are variable, with a minimum of three separate origins of this pod type in each of these clades. What was thought to be two separate origins of lomented pods in Adesmieae and Aeschynomeneae is now considered at least six origins combined with at least two reversals, and not counting polymorphisms.
New taxonomic evidence
In contrast to the above, a few previously overlooked characters are shown by analysis of combined molecular and nonmolecular data to be taxonomically informative. Short shoots (character 2 in Appendix B) evolved only once in the clade containing Pictetia, Ormocarpum, and Ormocarpopsis (also Peltiera). However, the support for this clade is moderate (Fig. 5), both in this analysis, and in those of Beyra-M. and Lavin (1999)
and Lavin et al. (2000)
. Bilabiate calyx lobes (state 2 of character 19 in Appendix B) mark the monophyly of the clade containing Aeschynomene sect. Aeschynomene, Smithia, Kotschya, Humularia, Cyclocarpa, Soemmeringia, Bryaspis, and Geissaspis. In contrast to short shoots, this calyx morphology marks a very well-supported clade (Fig. 5). The other nonmolecular characters with a high retention index (Table 1), however, either mark small clades (e.g., characters 13 and 46 and the clade with Brya and Cranocarpus), or have homoplasy that was underestimated because of scoring polymorphic taxa (e.g., see characters 39 and 40 in Appendix B).
The aeschynomenoid root nodule (Fig. 6, character 55 in Appendix B) is the most notable nonmolecular character in that it is inferred to be a synapomorphy for the dalbergioid clade. The idea that nodule morphology could be a useful character in legume taxonomy was pioneered by Corby (1981)
. He described a number of shapes, named according to the genus from which he had most observations. The aeschynomenoid type has as its main feature a small oblate nodule (transverse diameter greater than axial) with determinate growth. Corby noted that aeschynomenoid nodules are often associated with fine rootlets, but his otherwise excellent drawings omitted these "for clarity." Such nodules were found primarily in the tribes Adesmieae, and Aeschynomeneae, but also in some members of the Abreae, Dalbergieae, Phaseoleae, and Robinieae (Corby, 1988
). On his retirement, Corby kindly gave the Sprent laboratory his collection of preserved nodules. These were used, together with new material, for more detailed structural studies. As a result, the definition of an aeschynomenoid nodule has been adapted to include additional features. In particular, this nodule is always associated with a lateral or (in the case of stem nodules) adventitious root. The central infected tissue contains few or no uninfected cells. Differentiated infection threads are not involved in the process of infection, which (where studied in detail) takes place at the lateral root junction (Sprent, Sutherland, and Faria, 1989
). All nodules of the tribe Aeschynomeneae that have been examined conform to this description, together with ten genera of the Dalbergieae: Centrolobium, Dalbergia, Etaballia, Geoffroea, Machaerium, Platymiscium, Platypodium, Riedeliella, Tipuana, and Pterocarpus (two Brazilian species, P. rohrii and P. santalinoides are not known to nodulate). The evidence for Adesmia, Brya, and Cranocarpus, although slightly less detailed, is entirely consistent with the revised description of aeschynomenoid nodules.
|
). Two genera of the dalbergioid clade that do not nodulate are Chaetocalyx and Nissolia (Faria and Lima, 1998
). Both of these are lianes. Notably, a group of species in Acacia with a semiscandent habitat cannot nodulate (Harrier et al., 1997
). These acacias have retained some of the characters associated with nodulation, such as some of the nod genes, and the ability to stimulate rhizobial attachment to roots. It was thus suggested that they may have lost the ability to nodulate because, living on the forest margins, they were not nitrogen limited (Harrier, 1995
). It would be interesting to carry out similar tests on Chaetocalyx and Nissolia as one of their principal habitats is forest margins.
It is now generally agreed that nodulation in legumes may have evolved more than once (Sprent, 1994
; Soltis et al., 1995
). One of these nodulation events involved an infection process through a wound, such as where a lateral or an adventitious root emerges. Compared with the more familiar root hair infection pathway (see Sprent and Sprent, 1990
for details), this pathway is simpler, involving less complex recognition systems. Apart from some species of the mimosoid genus Neptunia (James et al., 1992
), this wound infection pathway is associated with only aeschynomenoid nodules. In Neptunia, however, nodule processes subsequent to infection involve production of infection threads and development of an indeterminate nodule.
Our phylogenetic results are in agreement with molecular and biochemical evidence that nodule structure and infection site are largely plant determined (e.g., Gualtieri and Bisseling, 2000
). Given a phylogenetic lineage, nodule morphology and infection processes are generally the same regardless of which species or genus of rhizobia is involved (six genera of bacteria nodulating legumes are now recognized, and they are collectively known as rhizobia). Another general inference is derived from the observation that all species of the genus Aeschynomene that have stem nodules are nodulated by photosynthetic rhizobia (Molouba et al., 1999
). Given that the aeschynomenoid root nodule has an unelaborated morphology and infection mode, the ancestral rhizobial form could have been photosynthetic. As legumes moved into drier areas, nodules developed on roots and lost photosynthetic ability (Sprent, 1994
).
A phylogenetic classification
The dalbergioid legumes are similar to a group of Papilionoideae that includes also Amorpheae and Dipterygieae. They share a distinctive combination of a base chromosome number of x = 10 (Goldblatt, 1981
), wood with uniseriate stored rays, vegetative growth with glandular punctae, flowers with fused keel petals or staminal filaments, and seeds that do not accumulate nonprotein amino acids (derived from Beyra-M. and Lavin, 1999
). The dalbergioids differ and are apomorphically defined (sensu de Queiroz and Gauthier, 1994
) as having glandular-based trichomes on vegetative or floral organs, a well-developed abaxial calyx lobe, and the "aeschynomenoid" root nodule. All of these traits have been secondarily transformed in some constituents of the dalbergioid clade (see characters 11, 19, and 55 in Appendix B; also Table 1).
The dalbergioid clade is distinguished more by molecular than nonmolecular data. It is another legume example of a cryptic clade, like "Neo-Astragalus" (Wojciechowski et al., 1993
) and the "temperate herbaceous clade" (Sanderson and Wojciechowski, 1996
). Regardless, it is informally recognized here as a distinctive taxonomic group. Furthermore, the three major constituent subclades are informally recognized and Appendix C enumerates the 44 current dalbergioid genera accordingly. The three subclades of dalbergioids are:
The Adesmia clade
This includes the genera Adesmia (of tribe Adesmieae; Polhill, 1981f
) and Poiretia, Amicia, Zornia, Chaetocalyx, and Nissolia of the tribe Aeschynomeneae. This clade is apomorphically defined as having an herbaceous growth habit (modified in some descendants—character 1), leaves with few opposite leaflets (evolved in parallel in Arachis and close relatives—character 8), and pedicels confluent with the calyx (modified only in a few species of Nissolia— character 17). A node-based definition (sensu de Queiroz and Gauthier, 1994
) includes all descendants from the common ancestor of Adesmia and Amicia.
The Dalbergia clade
This includes Dalbergia and Machaerium (of tribe Dalbergieae; de Candolle, 1825
; Polhill, 1981d
), and the following genera of Aeschynomeneae (sensu Rudd, 1981a
): Aeschynomene (all infrageneric taxa), Soemmeringia, Cyclocarpa, Kotschya, Smithia, Humularia, Bryaspis, Geissaspis, Weberbauerella, Diphysa, Pictetia, Ormocarpum, Ormocarpopsis, and Peltiera. This clade is apomorphically defined as having diadelphous staminal filaments splitting readily or tardily into two flanges, usually in a 5 + 5 arrangement (polymorphic with a 9 + 1 diadelphous condition in many species and occasionally monodelphous in Machaerium—character 26), and a persistent staminal flange that in some cases reflexes upward above the developing fruit (character 28). A node-based definition includes all descendants from the common ancestor of Dalbergia and Cyclocarpa.
The Pterocarpus clade
This includes Pterocarpus, Tipuana, Platypodium, Reideliella, Centrolobium, Grazielodendron, Paramachaerium, Ramorinoa, Inocarpus, Etaballia, Platymiscium, Cascaronia, Fissicalyx, Geoffroea from Dalbergieae; Brya and Cranocarpus from Desmodieae; and Fiebrigiella, Chapmannia, Stylosanthes, Arachis, and Discolobium from Aeschynomeneae. This clade is apomorphically defined as having commonly caducous bracteoles (character 18) and seedlings producing a simplified eophyll (secondarily transformed in Arachis and close relatives—character 45). A node-based definition includes all descendants from the common ancestor of Pterocarpus and Riedeliella.
Although data from matK/trnK, trnL, and ITS/5.8S were not combined in a single analysis, results from individual analyses showed significant consensus combined with no significant conflict. The combined matK/trnK and nonmolecular analysis yielded very robust results to support the conclusions outlined above. This study demonstrates that matK/trnK sequences provide excellent resolution at the broadest phylogenetic levels dealt with in this study. This same locus, along with ITS/5.8S, gives excellent resolution to within and among closely related genera. In contrast, trnL provides the least resolution. Ultimately, this study provides a framework for future studies that deal taxonomically with individual dalbergioid genera. There is now sufficient data from which to guide the choice of potential sister groups or outgroups in such studies.
|
|
|
|
|
|
|
|
|
|
|
|
APPENDIX |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITEDAPPENDIXAPPENDIX |
|---|
) and the trace option in MacClade (Maddison and Maddison, 1999
).
Vegetative characters
1. Habit: 0) woody (trees to shrubs), 1) herbaceous (subshrubs to herbs), 2) twining and herbaceous, 3) twining and woody. Predominantly herbaceous genera sometimes include subshrubby species, whereas woody genera usually do not, thus explaining the coding for state number 1. A herbaceous habit arose independently in the following clades: one represented by Fiebrigiella and Arachis, another by Chaetocalyx and Poiretia, and one by Weberbauerella and Kotschya. The twining herbaceous habit is restricted to the Adesmia clade where it is known from some species of Poiretia (Rudd, 1972c
) and all Chaetocalyx (Rudd, 1958
) and Nissolia (Rudd, 1956
). A twining woody habit occurs in polymorphic condition in the clade with Dalbergia and Machaerium.
2. Short shoots: 0) absent or not regularly present and then not covered by persistent stipules, 1) regularly present and covered by distichously arranged persistent stipules from the axils of which are born the inflorescence (Fig. 7). The short shoot condition is restricted to the clade including all descendants of the most recent common ancestor of Pictetia and Ormocarpopsis. Very similar short shoots were described for Poitea (tribe Robinieae; Lavin, 1993
), which is also from the Greater Antilles.
3. Stipule modifications: 0) attached to stem at base (basifixed) and foliaceous, 1) attached to stem in the middle and foliaceous (peltate or medifixed), 2) basifixed and lignescent. Medifixed stipules are referred to as appendiculate (e.g., Rudd, 1981a
) and are evolved independently in a clade including Aeschynomene sect. Aeschynomene, Cyclocarpa, Humularia, Geissaspis, Smithia, and another including just Zornia. Lignescent stipules evolved independently in polymorphic condition in the liana-forming species of Machaerium, in most species of Brya, and in all species of Pictetia. In Brya, the leaves of the long shoot are entirely transformed into a single spine.
4. Pseudopetiole: 0) absent, 1) present (Fig. 8). A pseudopetiole is traditionally defined as a petiole with stipules attached. It is here described as a pulvinus (leaf base) that is projected away from the main axis of the stem. The stipules are attached to this projected portion of the stem, and they superficially appear as if they are adnate to the petiole. The pseudopetiole evolved independently in a clade including just Adesmia, and another including Arachis and Stylosanthes.
5. Leaf rachis in cross section: 0) terete, 1) with a single continuous groove (canaliculate). A terete leaf rachis is recorded from Discolobium, Dalbergia, Machaerium, and Ormocarpopsis, Peltiera, Platymiscium, Centrolobium, Grazielodendron, Etaballia, Fissicalyx, Peltiera, and Pterocarpus, and in polymorphic condition from Ormocarpum, Aeschynomene (all subgroups) and closely related genera (Cyclocarpa, etc.). Grooved leaf rachises occur in the rest of the genera, except where the leaves are uniformly sessile, as in Brya and Inocarpus, and this trait is then scored as inapplicable. Otherwise, leaf rachises vary continuously between narrowly grooved and distinctly canaliculate. The motivation for using this trait is that terete leaf rachises are shown to be derived (but in polymorphic condition) in two clades: that including all descendents but Pictetia of the most recent common ancestor of Dalbergia and Ormocarpopsis, and that including most descendants of the recent common ancestor of Platymiscium and Pterocarpus.
6. Distal end of leaf rachis: 0) terminated by a leaflet, 1) not terminated by a leaflet (a mucro is often present). A leaf rachis not terminated by a leaflet is found in the large clade including Aeschynomene sect. Aeschynomene, Cyclocarpa, Humularia, Soemmeringia, Kotschya, Smithia, Geissaspis, and Bryaspis. This type of leaf also has evolved independently in the outgroup samples of Dipterygeae (Dipteryx and Pterodon), the clade including Amicia, Zornia, Adesmia, Arachis, and Poiretia, the clade including just Aeschynomene sect. Ochopodium, and the clade including Stylosanthes and Arachis.
7. Number of leaflets per leaf: 0) leaves unifoliolate/simple, 1) leaves tri- to 20-foliolate, 2) leaves more than 20-foliolate. State zero occurs uniformly in Etaballia, Inocarpus, and Brya, and in polymorphic condition in Cranocarpus. State two is restricted to just the Dalbergia clade where it occurs uniformly in Weberbauerella, and predominantly so (i.e., polymorphic) in Machaerium, Dalbergia, and all the sections and series of Aeschynomene (Aeschynomene, Viscidulae, Pleuronerviae, and Scopariae). This state is capturing "fern-like" leaves where the leaflets abut laterally, are narrowly elliptic, and have parallel lateral margins. Simple leaves are scattered throughout but with most occurrences (usually in polymorphic condition) in the Pterocarpus clade (Discolobium, Etaballia, Inocarpus, Platypodium, Byra, and Cranocarpus).
8. Leaflet arrangement: 0) alternate, 1) opposite. Two large clades have evolved opposite leaflets independently. One includes Adesmia, Chaetocalyx, Nissolia, Poiretia, Amicia, Zornia, and the other includes Fissicalyx, Fiebrigiella, Chapmannia, Stylosanthes, and Arachis. Opposite leaflets have evolved sporadically mostly within the Pterocarpus clade (Grazielodendron, Riedeliella, Cranocarpus, Paramachaerium), and rarely in the Dalbergia clade (Smithia). The genera with uniformly simple or unifoliolate leaves (e.g., Etaballia, Inocarpus, Brya, and Ramorinoa) were marked inapplicable. The species of Cranocarpus with imparipinnate leaves have opposite leaflets, and this condition is used to represent the genus. A terminal taxon is scored for opposite leaflets if all constituent species predominate with this condition. A terminal taxon is scored for a polymorphic condition only if some constituent species have uniformly opposite leaflets and others have uniformly alternate leaflets.
9. Leaflet base: 0) symmetric, 1) asymmetric. The asymmetric state is restricted to the Dalbergia clade, where it has evolved independently and polymorphically in Pictetia and Aeschynomene (all subgroups except Scoparia) and uniformly in Humularia, Bryaspis, Geissaspis, Kotschya, and Smithia. An asymmetric base of the leaflet is correlated with an eccentric midrib and probably related to a nyctinastic leaflet movement that involves a forward twisting and folding of each leaflet. This "forward-folding" type is very similar to the leaflet movements in legume subfamilies Mimosoideae and Caesalpinioideae, as well as the papilionoid genus Sesbania, and it has been observed in species of Aeschynomene, Arachis, Diphysa, Dalbergia, and Machaerium.
10. Tannin deposits on the abaxial surface of dried leaflets: 0) absent, 1) present. Tanniniferous patches on dried leaflets have evolved independently in the clade including Arachis, Stylosanthes (polymorphic in these first two), and Chapmannia (this is the subtribe Stylosanthinae of Rudd, 1981a
) and in two genera endemic to Madagascar, Ormocarpopsis and Peltiera (Labat and Du Puy, 1996, 1997
). Reddish tannin deposits usually occur in reticulate patterns demarcating individual epidermal cells. In Ormocarpopsis and Peltiera, they can be concentrated along the leaflet midrib.
11. Glandular-based trichomes: 0) absent, 1) present (Figs. 9, 10). This type of trichome is a synapomorphy for the dalbergioid group, where it is found on the stems, leaves, inflorescence, or ovary. Although synapomorphic, the glandular-based trichomes have been secondarily lost several times in each of the Adesmia, Dalbergia, and Pterocarpus clades. In addition to most genera of the formally recognized tribe Aeschynomeneae, glandular-based trichomes are found in Centrolobium, Grazielodendron, Ramorinoa, Etaballia, Riedeliella, Fissicalyx, Paramachaerium, Peltiera, and polymorphic in Brya, Cranocarpus, Dalbergia, and Machaerium.
12. Pustular glands: 0) absent, 1) present (Fig. 11). The latter condition is thought to be a derivation of the general dalbergioid trait of punctate glands (all members of the ingroup and outgroup possess punctate glands on the leaflets). There has been further development in the size and color of the common punctate gland such that they protrude outward from the plane of the leaflet, calyx, or ovary and are brownish red to blackish in color. Pustular glands are known from genera outside the dalbergioid clade (Acosmium, Myrospermum, Amorpha, Apoplanesia, Dipteryx, and Pterodon), and have evolved in four separate instances within the dalbergioid clade (Geoffroea and Cascaronia; Poiretia, Amicia, and Zornia; Weberbauerella; and Centrolobium).
13. Stipitate glands: 0) absent, 1) present from non-glochidiate trichomes, 2) present from microscopically glochidiate trichomes (Fig. 12). Such glandular trichomes are usually present on stems or leaves, but can also occur on ovaries and pods. Stipitate glands have evolved in the clade including Brya, Cranocarpus, and Grazielodendron (uniquely from glochidiate trichomes in the first two genera), and in polymorphic condition in the clade including Adesmia, Chapmannia, and Stylosanthes. In Brya and Cranocarpus, stipitate glands are found, in addition to the foliage, on the ovary where they persist with the mature fruit. The high tree scores for this character (Table 1) do not account for the optimizations of polymorphic codings where Chapmannia, Stylosanthes, and Adesmia were assigned state zero during parsimony analysis.
Inflorescence characters
14. Inflorescence position: 0) axillary, 1) terminal. The first state corresponds to leafy flowering branches that are indeterminate with vegetative growth from the apical meristem. The second refers to leafy flowering branches whose growth is terminated by the inflorescence. The relatively high scores (Table 1) reflect the uniform occurrence of state one in the clade including Apoplanesia and Amorpha, and in the two species of Geoffroea. Other cases of independent evolution but in polymorphic condition include Reideliella, most outgroup genera, and sporadically throughout the Dalbergia clade (Aeschynomene subgroups, Kotschya, and Smithia).
15. Inflorescence type: 0) racemose, 1) axillary subumbel, 2) solitary axillary flowers, 3) helicoid cymes. Helicoid cymes have evolved several times but in all cases within the Dalbergia clade (Dalbergia, Machaerium, Aeschynomene, Kotschya, and Smithia). They appear to arise readily from any inflorescence condition (i.e., note the polymorphic codings for most of these genera). In the axillary subumbel, the internodes of the rachis are telescoped down almost completely, as in Chaetocalyx and Nissolia. Solitary flowers have evolved independently and uniformly in Brya and the clade with Arachis and Stylosanthes. Notably, polymorphic codings for this character are highly localized to the genera in the clade that includes the most recent common ancestor of Dalbergia and Ormocarpopsis.
16. Floral bracts: 0) smaller than the flower or fruit, 1) larger than the flower or fruit. Large floral bracts have evolved independently in Zornia, and the clade including Bryaspis, Geissaspis, and Humularia. These two states are markedly discontinuous where the smaller bract is barely visible.
Floral characters
17. Pedicels: 0) articulated with the calyx, 1) confluent with calyx, 2) absent, flowers sessile. The Adesmia clade is marked by pedicels confluent with the calyx, with the exception of a very few species of Nissolia. State zero is most common among the rest of the dalbergioid clade and could be the ancestral condition to the Dalbergia and Pterocarpus clades. If so, then a transition to pedicels confluent with the calyx has occurred many times independently (Reideliella, Ramorinoa, Centrolobium, Brya, Cranocarpus, Weberbauerella, and Geissaspis, Bryaspis, and Humularia). Sessile flowers have evolved three times, once in Chapmannia, Arachis, and Stylosanthes (the subtribe Stylosanthinae of Rudd, 1981a
), and again in Etaballia and Inocarpus.
18. Bracteoles: 0) persistent, 1) caducous, 2) not or irregularly produced. Bracteoles persisting paired at the end of the pedicel after abscission of the flower or with the developing or mature fruit are common to the dalbergioids. Caducous signifies that the bracteoles fall before the flower aborts or before the pod begins to form. Caducous bracteoles are highly localized in the clade that includes all descendants of the most recent common ancestor of Pterocarpus and Platymiscium. Such bracteoles have also evolved independently in Geoffroea, Riedeliella, and several of the outgroups. Bracteoles occur irregularly (i.e., mostly singly and variously along the pedicel) or not at all in four separate clades: one including Weberbauerella, another with Humularia, Geissaspis, yet another with Amicia, Poiretia, Zornia, Chaetocalyx, and Nissolia, and finally in Cascaronia.
19. Calyx lobe fusion: 0) five more or less equally spaced lobes, 1) five separate lobes but with the abaxial one (lower or carinal) the largest and separate from laterals, 2) a two-lipped calyx with the abaxial lobe fused completely or nearly so to the two lateral lobes, and the upper two lobes completely fused, 3) Dipteryx type, 4) Fissicalyx type, 5) Inocarpus type. Character state one is synapomorphic for the dalbergioid clade, and it is most distinctive developmentally with the abaxial sepal initiating with the larger size and faster growth rate relative to the other sepals (Klitgaard, 1999a
). The most notable derivation from this condition within the dalbergioids is state two, which occurs in the clade with Aeschynomene sect. Aeschynomene, Cyclocarpa, Soemmeringia, Kotschya, Smithia, Geissaspis, Bryaspis, and Humularia (Aeschynomeneae subtribe Aeschynomeninae of Rudd, 1981a
). The Dipteryx type occurs in Dipteryx, Pterodon, and Amicia zygomeris, where the upper two calyx lobes are greatly enlarged, contrasting with the diminutive lower three lobes. The Fissicalyx type evolved only in Fissicalyx, where all the calyx lobes occur as an upper lip (spathaceous). The Inocarpus type has three lips, the lower formed by the carinal lobe, and two lateral lips formed by one lateral and one vexillar lobe. Also, the Socotran species of Chapmannia have yet another type where the upper lip of a bilabiate calyx comprises the two upper and two lateral calyx lobes, and the lower lip comprises just the carinal lobe. Chapmannia, however, was scored for state one because it represents the ancestral state for the genus (see the Chapmannia phylogeny in Lavin et al., 2000
). Similarly, the ancestral state for Pictetia is state one (Beyra-M. and Lavin, 1999
).
20. Hypanthium: 0) not well developed, petals and stamens arising at the base of the ovary, 1) short-tubular, petals and stamens arising from a rim positioned above the ovary base but not above the ovary itself, 2) long-tubular, where petals and stamens arise from a rim located above the ovary. The calyces of Acosmium, Apoplanesia, Amorpha, and Etaballia have a poorly developed hypanthium (the last genus represents the only reversion to a loss of the hypanthium among dalbergioid legumes). Among the dalbergioids, state one predominates and is ancestral. State two is confined to the clade including Chapmannia, Arachis, and Stylosanthes.
21. Petal coloration: 0) predominantly whitish to reddish or violet, 1) predominantly yellow. The large majority of dalbergioid legumes have yellow petals, and this is inferred to be ancestral. Notable exceptions include the clade with Dalbergia and Machaerium (polymorphic), as well as Grazielodendron, Paramachaerium, Ormocarpum (polymorphic), and Adesmia (the species with solitary axillary flowers) where whitish to violet petals are common.
22. Corolla symmetry: 0) bilateral (papilionoid), 1) nearly radial. State zero predominates among dalbergioids and indeed most papilionoids. Notably, a nearly radially symmetric flower has evolved independently four times: once each in Inocarpus, Etaballia, Reideliella, and the clade with the samples of Amorpheae (Apoplanesia and Amorpha). Nearly radially symmetric flowers have also evolved independently in the four species of Pictetia where state zero is considered ancestral (Beyra-M. and Lavin, 1999
).
23. Petal morphology: 0) petals abruptly differentiated into a blade and claw (Figs. 13–15), 1) petals ligulate, the claw and blade not distinguishable (Fig. 16). State one evolved separately in Etaballia and Inocarpus. This character is not dependent on character number 22 because Amorpheae, Reideliella, and four species of Pictetia have a nearly radial flower symmetry with petals differentiated into a blade and claw.
24. Keel petals: 0) free, 1) connate, at least along the carinal margin if not to near the tip. Free keel petals in papilionoid legumes have been the hallmark of the tribes Swartzieae and Sophoreae. Acosmium and Myrospermum, traditionally placed in the tribe Sophoreae, have free keel petals. Among the dalbergioid legumes, fused keel petals represent the ancestral condition that has reverted back to the free condition only in Etaballia, Geoffroea, Riedeliella, Platypodium, and Tipuana (all confined to the Pterocarpus clade).
25. Wing petals: 0) smooth, 1) crimped. Crimped wing petals are distinctly much broader than the adjacent keel petals. The evolution of such wing petals has occurred in the clade including Paramachaerium, Pterocarpus, Ramorinoa, Paramachaerium, Tipuana, and Platypodium, and separately in that including Geoffroea.
Androecial characters
26. Staminal filaments: 0) all free from the base, 1) diadelphous 9 + 1, 2) open monodelphous, 3) closed monodelphous, 4) diadelphous [5 + 5, 5 + 4 + 1, or 4 + 1 + 4 + 1] with at least two phalanges of fused filaments. State two is the inferred ancestral condition of the dalbergioid legumes. State four is synapomorphic for the Dalbergia clade (though species of Ormocarpum, Pictetia, Diphysa, Machaerium, and Dalbergia are polymorphic). State four, however, has evolved independently in Platypodium and Discolobium (both of the Pterocarpus clade). The free stamens of Adesmia are inferred to represent a reversion from an open monodelphous condition. State one is uncommon among dalbergioids and is monomorphic only among some members the Pterocarpus clade (Grazielodendron, Geoffroea, and Ramorinoa). The diadelphous 9 + 1 condition is associated with weakly developed basal fenestrae (Klitgaard, 1999a
).
27. Anther size and attachment: 0) monomorphic, basi- to dorsi-fixed, 1) dimorphic, the smaller anthers usually dorsifixed, the larger basifixed. Character state one evolved independently in the clade with Amicia (polymorphic), Poiretia, and Zornia, and again in that with Arachis and Stylosanthes. Dimorphic anthers also have other sporadic occurrences, such as in Aeschynomene genistioides (Aeschynomene sect. Ochopodium; Rudd, 1967, 1972a
), the monotypic Aeschynomene subgen. Bakerophyton (Verdcourt, 1971
), and in a Mesoamerican clade of Platymiscium species (B. Klitgaard, unpublished data).
28. Staminal flange and filaments post-anthesis: 0) readily caducous, not persisting with the maturing fruit, 1) persistent on the abaxial side of fruit, 2) persistent on adaxial side of fruit. This trait is only partially conditional upon character number 27 (see Beyra-M. and Lavin, 1999
). Persistent stamens are diagnostic of the Dalbergia clade where the predominant condition is state one. State two occurs in a clade with Aeschynomene sect. Aeschynomene, Kotschya, etc. Persistent stamens evolved separately in Brya, Cascaronia, and several outgroup genera.
Gynoecial characters
29. Locule: 0) encompassing nearly the entire length of the ovary, 1) confined to the basal end of the ovary. The locule is situated just above the stipe in state one, and a large portion of the distal end is solid. All five occurrences of this state are inferred to be cases of independent evolution (Vatairea, Vataireopsis, Tipuana, Centrolobium, and Paramachaerium).
30. Nectary disk: 0) absent; 1) present. A nectary disk surrounding the base of the ovary is known from Paramachaerium (Rudd, 1981a
), most species of Ormocarpum (M. Thulin and M. Lavin, unpublished data), and occasionally in Machaerium (Klitgaard, 1999a
). The retention index is undefined in this character (Table 1) because Machaerium and Ormocarpum were assigned an ancestral state of zero.
Fruit and seed characters
31. Pod valves: 0) loments present during early stages of fruit development, 1) loments present by late stages, 2) valves continuous. Articulations forming late during pod development occur in Ormocarpum, Pictetia, Diphysa, Chaetocalyx, and Nissolia. Some species in the first of these three genera form inarticulate pods. Only in the Adesmia clade is the lomented condition uniformly present. Both of the Dalbergia and Pterocarpus clades combine genera with articulate and inarticulate pods.
32. Pod margins: 0) straight, with no marginal constrictions between seeds 1) constricted between seeds. State one has evolved numerous times independently in Discolobium, Fiebrigiella, Brya and Cranocarpus (polymorphic), Amicia, and Giessaspis, Bryaspis, Humularia, Kotschya, and Smithia. Aeschynomene, Ormocarpum, and Diphysa are distinctively polymorphic for this character.
33. Stipe of mature pod: 0) absent to less than half the length of the calyx tube, 1) surpassing the length of the calyx tube. State one has evolved most uniformly in the clade with Dalbergia, Machaerium, Diphysa, Ormocarpum, Ormocarpopsis, Peltiera, and Pictetia. Among dalbergioids, state zero predominates only in the Adesmia clade. Otherwise, both states have been gained and lost on many separate occasions, particularly in the Pterocarpus clade.
34. Nervation of the mature pod valve in the region of the seed chamber: 0) primarily reticulate, 1) primarily longitudinally parallel. This trait has evolved once in the clade with Arachis, Stylosanthes, Chapmannia, and Fiebrigiella, (not Fissicalyx, however), and again in the clade with Chaetocalyx and Nissolia. Some species of Diphysa, Ormocarpum, and Pictetia have pods with strong longitudinal nerves, but these genera were optimized during analysis as having state zero.
35. Replum: 0) placental margin disarticulating with the pod valves or articles, 1) the valves or articles disarticulating separately from the persistent placental margin. The last state is gained independently in Adesmia sect. Muricatae, Cyclocarpa, and in species of Aeschynomene sect. Aeschynomene (e.g., A. villosa). This character had an undefined retention index (Table 1) because Adesmia and Aeschynomene were optimized for state zero.
36. Development of pod wings: 0) not winged, 1) wing from expansion of the ovary wall, 2) wing from expansion of the ovary sutures, 3) wing from attenuation of the distal end of the ovary (i.e., the style), 4) winged from attenuation of the proximal end of the ovary (i.e., the stipe). This character is derived from Lima's (1990)
developmental work on samaroid fruits of tribe Dalbergieae. He distinguished wings whose area of origin was the ovary walls (state one); wings with an origin of the ovary sutures (state two); and wings with an origin from the distal end of the ovary (state three). Lima considered Vatairea and Vataireopsis to have a separate state, with wings derived from the solid distal portion of the ovary. This reflects the different morphology of the gynoecium in these two genera (see state one of character 29). We consider that the origin of the wing in these taxa is merely from the distal end of the ovary, and thus they are coded with state three. A further modification is that we consider the basal wing of Platypodium to be derived from an expansion of the stipe (state four). Developmental anatomical work could confirm these distinctions. State one has evolved independently in both the Dalbergia (Dalbergia and Weberbauerella) and Pterocarpus clades (Platymiscium, Cranocarpus, Grazielodendron, Ramorinoa, Pterocarpus, Fissicalyx, and Riedeliella). State three has evolved in every occurrence separately (Vatairea, Vataireopsis, Nissolia, Machaerium (polymorphic), Tipuana, Centrolobium, and Paramachaerium).
37. Inner epidermis and endocarp: 0) lignescent, 1) spongy and adhering to the mature seeds. State one evolved in the clade with Chaetocalyx and Nissolia, and again in that with Pictetia, and perhaps again in Peltiera (the sister genus of Ormocarpopsis—see Labat and Du Puy, 1997
).
38. Mesocarp: 0) lignescent, 1) spongy, 2) fleshy. State one arose independently and uniformly in Pictetia and Fiebrigiella, and sporadically in Ormocarpum, Chapmannia, Nissolia, and Chaetocalyx. State two occurs in the fleshy vertebrate dispersed fruits of Dipteryx, Andira and Geoffroea, all instances of independent evolution. Polymorphic terminals were optimized for state zero, effectively underestimating the actual levels of homoplasy.
39. Exocarp: 0) adnate to the mesocarp, 1) loosely attached to mesocarp, 2) separate from the mesocarp by the formation of a distinct air chamber. This last trait occurs in many species of Diphysa and a few species of Nissolia (e.g., N. leiogyne). State one is characteristic of Ormocarpopsis. The high tree scores for this character (Table 1) resulted from state zero being assigned to the polymorphic terminals Diphysa and Nissolia during parsimony analysis.
40. Pod coiling: 0) coiled in a forward directed manner, 1) not coiled, 2) coiled in a laterally directed manner. The forward coil of the pod is confined to Discolobium, whereas the lateral coil has evolved in Cyclocarpa and various species of Aeschynomene sect. Aeschynomene and Ormocarpum. Although the lateral coil is restricted to members of the Dalbergia clade, state one was assigned to the polymorphic terminals Aeschynomene and Ormocarpum during parsimony analysis, resulting in high tree scores (Table 1).
41. Pod valve ornamentation: 0) not present, 1) multiseriate trichomes, 2) crests and bumps. Multiseriate trichomes persisting on the mature pod valve have evolved in many separate occasions throughout the dalbergioid legumes, as in Adesmia (polymorphic), Ormocarpum (polymorphic), Brya, and Centrolobium (where they become spinose). Pod valves with crests or bumps have evolved once in the clade with Poiretia, Amicia, and Zornia, and again in polymorphic condition among various species of Aeschynomene sect. Aeschynomene. The polymorphic terminals Adesmia, Ormocarpum, and Aeschynomene were assigned state zero during parsimony analysis, thus resulting in relatively high tree scores (Table 1).
42. Seed shape: 0) lenticular to spherical with a centrally placed hilum, 1) reniform with a central recessed hilum, 2) longitudinally elongate with the hilum placed toward the end toward the style. The last condition is characteristic of most dalbergioids and indeed ancestral to that clade. However, state two has evolved independently in Dipterygeae (Dipteryx and Pterodon), Hymenolobium, Vatairea (polymorphic), and Vataireopsis. Among dalbergioids, Aeschynomene, Kotschya, Smithia, and Platymiscium have reniform seeds (three separate origins), and Ormocarpopsis and Peltiera have spherical seeds.
43. Orientation of the seed in the fruit: 0) longitudinal, 1) oblique to transverse. Oblique to transverse orientation of seeds is confined to a subclade including Platymiscium, Centrolobium, Paramachaerium, Pterocarpus, Ramorinoa, and Tipuana (Lima, 1990
). Such seeds have also evolved independently in Hymenolobium (polymorphic).
Seedling characters
44. Position of the eophylls: 0) alternate, 1) opposite. Among dalbergioids, opposite eophylls are confined to the Pterocarpus clade where they are known from Platymiscium, Grazielodendron, Ramorinoa, Centrolobium, and Geoffroea.
45. Number of leaflets in the first eophyll: 0) one, 1) more than one. Dalbergioids commonly have eophylls that are not strongly differentiated from the adult leaves (i.e., multifoliolate). The Pterocarpus clade is exceptional in having all known instances where the eophylls are unifoliolate. Data for characters 44 and 45 for Ramorinoa came from Burkart (1952
, p. 238).
Pollen characters
46. Aperture type: 0) tricolporate, 1) periporate. Tricolporate apertures are the general and most common type in legumes. Among the dalbergioids, periporate pollen is known from only Brya and Cranocarpus.
47. Pollen pore: 0) without an operculum, 1) with an operculum. An operculum is a distinctly delimited ectexinous structure that covers the ectoaperture, which in the case of all dalbergioids means the colpus. State one has been gained independently many times throughout all three principal clades of the dalbergioid legumes.
48. Colpi (the polar region): 0) colpi short, not anastomosing at the poles of the pollen grain, the polar region entire, 1) colpi longer, the ends of colpi anastomosing, forming syncolpi. State one evolved independently and uniformly in Humularia and Vataireopsis. This state is polymorphic for Aeschynomene, Kotschya, and Smithia. Thus, state one is confined to the Dalbergia clade among the dalbergioid legumes.
49. Wall stratification (Guinet and Ferguson, 1989
): 0) well-developed endexine and footlayer, 1) thickening of the endexine at least at the apertures combined with a reduction in the foot layer, 2) reduction of the endexine combined with a thickening of the foot layer, 3) reduction of the endexine and foot layer combined with an elongation of the columellae. State one is most common among the dalbergioids and is inferred to be ancestral in this clade. State two evolved independently in Adesmia and the outgroup Myrospermum. State three evolved once in the clade with Geissaspis and Bryaspis.
Wood characters
50. Ray size: 0) three or more cells wide, and taller than 20 cells high, 1) 1–2 cells wide and less than 15–20 cells high. Many of the dalbergioid genera have narrow short rays (state one). Good examples include Platymiscium, Fissicalyx, and the nondalbergioid Dipteryx. Outgroup genera have storied rays that are larger than this. Wood characters were scored from examination of slides in the collections at the Jodrell Laboratory, Kew, and at the Forest Products Laboratory, Madison, Wisconsin, USA, and by reference to descriptions and photographs in Baretta-Kuipers (1981)
, Gasson (1994, 1999)
, Miles (1978)
, and Détienne and Jacquet (1983)
. Wheeler, Bass, and Gasson (1989)
provide thorough definitions for all of the wood characters used in this analysis. Details on the wood anatomy of Chaetocalyx, Nissolia, Poiretia, Amicia, Zornia, Chapmannia, Arachis, Stylosanthes, Soemmeringia, Smithia and Geissaspis come from Cumbie (1960)
. Unfortunately, the information is presented in such a way that only a few character states can be coded. Amorpha fruticosa has been illustrated and described by Schweingruber (1990)
, Adesmia horrida by Roig (1986)
, Discolobium by Cozzo (1949, 1950)
, and Paramachaerium by Brizicky (1960)
. No information on the wood anatomy is available for Riedeliella, Cranocarpus, Fiebrigiella, Cyclocarpa, Kotschya, Bryaspis, Humularia, Weberbauerella, Ormocarpum, Ormocarpopsis, and Peltiera.
51. Ray arrangement: 0) not storied, 1) storied. In legumes, storied rays, axial parenchyma, and adjacent vessels are common and can be observed in tangential longitudinal section. Although considered a very useful anatomical character, both diagnostically and cladistically, there are many legume genera with storied rays that are irregular, or obvious in short rays and less so in taller rays which may be axially fused. Storied rays are particularly strongly developed in Dipteryx, Pterocarpus, Platymiscium, Grazielodendron, Etaballia, Inocarpus, Dalbergia, Machaerium, and Aeschynomene, all of which have short rays. The taxa with larger rays often do not exhibit such regular storied arrangement, and axial fusion is often the cause, as in species of Acosmium.
52. Composition of cells in rays: 0) homocellular, 1) heterocellular. This feature is observed in radial longitudinal section. Homocellular rays are composed entirely of procumbent ray cells. Heterocellular rays in legumes are composed mainly of procumbent cells, but there are also some square or upright cells, usually in a row or rows at the ray margins (i.e., at the top or bottom of a ray). These two character states are not mutually exclusive. Juvenile wood often tends to be more heterocellular than mature wood, and it is not always apparent where exactly a wood sample was taken from if the pith in the stem is not included.
53. Crystals in ray cells: 0) absent, 1) present in some ray cells. Prismatic crystals of calcium oxalate are found in many, if not most legumes. They are almost ubiquitous in chambered axial parenchyma strands, but in a few genera can also be found in ray cells. The main difficulty with this character is that if the crystals are rare they can be overlooked. They are searched for in radial longitudinal section, because they are even more difficult to find in tangential longitudinal section.
54. Axial parenchyma: 0) not abundantly aliform and confluent, 1) abundantly aliform and confluent. Axial parenchyma patterns in legumes are very difficult to code. All the legumes in this study have predominantly paratracheal parenchyma, with the addition of some apotracheal diffuse parenchyma in particularly Dalbergia and Platymiscium. This ranges continuously from scanty paratracheal, vasicentric, aliform, to confluent. In the opinion of one of us (Gasson), these all constitute one character. They could each be coded as character states, but virtually all wood samples in the legumes exhibit more than one condition. Unilaterally paratracheal parenchyma is found in some of the taxa, and probably forms part of this continuum. Banded parenchyma, which could be treated separately, may be an extreme form of confluent parenchyma, particularly if the bands are several cells wide. Some taxa in the study group do have narrow bands, but they are not distinguished here. The choice of the two character states above serves to separate four of the genera very well, but does not distinguish all the other complicated variations on the paratracheal theme exhibited by the taxa coded as zero. Aeschynomene is very different, in that it has such abundant parenchyma, that the fibers exhibit a winged-aliform appearance.
Nitrogen fixation character
55. Root nodule: 0) none produced, 1) produced as a non-aeschynomenoid nodule, 2) produced as an aeschynomenoid nodule (Fig. 6; Corby, 1981
; see discussion). State two is synapomorphic for the dalbergioid clade, although some genera in this clade are known not to produce nodules at all (i.e., Chaetocalyx and Nissolia), as is the case for some nondalbergioids (e.g., Myrospermum, Dipteryx, Pterodon, Vatairea, and Vataireopsis). Some outgroups produce nodules of a type other than aeschynomenoid (e.g., Acosmium, Poecilanthe, Andira, Hymenolobium, and Amorpha). Although lost within the dalbergioid clade (Table 1), the aeschynomenoid root nodule is not encountered elsewhere in the legume family. The stem (but not root) nodules of Sesbania rostrata (tribe Robinieae) are superficially similar, but they differ from the aeschynomenoid type in having an apical meristem, albeit ephemeral (J. Sprent, unpublished data). Three dalbergioid genera, Cyclocarpum, Geissaspis, and Paramachaerium, are known to produce nodules, but the exact type is unknown. These genera were variously coded as having missing data or state one. Such alternative coding did not affect how these genera were related with respect to the three major subclades of the dalbergioid clade. Future studies incorporating nodule morphology in a phylogenetic analysis will do well to recognize specific morphologies independent of nodule categories. Specifically, these would include characters such as the apical meristem (absent vs. present), infection site (associated with emergent rootlet or not), infection threads (absent vs. present), and central tissue (uniformly infected vs. uninfected). The aeschynomenoid type is defined as having the first state of each of these four characters. Regardless, this coding strategy would not change our findings because the dalbergioids would be nearly uniform in occurrence for the states of these four characters.
|
APPENDIX |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITEDAPPENDIXAPPENDIX |
|---|
The Adesmia clade
Adesmia DC. is diagnosed by stipules attached a pseudopetiole. Although also found in Stylosanthes and Arachis, the projected portions of the nodes of these two genera are nearly as long as the petiole. In Adesmia, the nodal projections extend to much less than half the length of the petiole. In addition, Adesmia uniquely combines free staminal filaments and lomented pods (Polhill, 1981f
). Adesmia comprises about 230 species centered in Chile and Argentina (Burkart, 1949, 1954, 1960, 1962, 1964, 1966, 1967
; Ulibarri, 1978, 1980, 1982a, b, 1984, 1987, 1990
). The genus contains two distinct monophyletic subgroups, according to ITS/5.8S sequence analysis (Fig. 3). One is marked by inflorescences of usually solitary axillary flowers with pedicels confluent with the calyx, stipules (or at least scars) that are connate around the stem, and pods that lack glandular-based trichomes, multiseriate trichomes, or the raised pericarp reticulations (e.g., Adesmia lanata and A. villosa). The second clade is characterized by inflorescences of terminal racemes, subumbels, or panicles, flowers articulated with the pedicel, stipules (or scars) that are not connate around the stem, and pod loments that commonly bear some type of ornamentation, for example, large glandular-based trichomes, long multiseriate plumose trichomes, or very prominent reticulate venation (e.g., Adesmia muricata and A. volckmannii). Phylogenetic analysis of ITS/5.8S sequence data strongly supports the monophyly of Adesmia, as does matK/ trnK.
Chaetocalyx DC. (Figs. 17–23) is paraphyletic with respect to Nissolia, an issue that is the focus of another study (M. Lavin and D. Prado, unpublished data). It possesses no autapomorphic traits and is characterized like Nissolia (with twining herbaceous stems and ebracteolate flowers) but lacking the sterile (usually samaroid) terminal loment of the mature pod. The glandular-based trichomes on the calyx of most species of Chaetocalyx are not diagnostic and the species of Chaetocalyx form a rather homogeneous assemblage. The supposedly obvious division between species with laterally flattened or winged fruits vs. those with terete fruits (as coded in Beyra-M. and Lavin, 1999
) is not resolved with 5.8S/ITS sequence analysis. Chaetocalyx includes 13 neotropical species centered in dry forests of South America (Rudd, 1958, 1972b, 1996
).
Nissolia Jacq. is derived from within Chaetocalyx (Figs. 2, 3, and 5) and characterized by the autapomorphy of pods with a sterile (usually samaroid) terminal loment (Figs. 24–28). This genus contains 13 species centered in tropical dry forests of Mexico and Central America (Rudd, 1956, 1970a, 1975b
). Chaetocalyx and Nissolia lack floral bracteoles, otherwise occurring among dalbergioids in Poiretia, Amicia, Zornia, Cyclocarpa, Humularia, Geissaspis, and Bryaspis.
Amicia Kunth occurs in Mexico, Ecuador, Peru, Bolivia, and Argentina (Rudd, 1981a
). This genus is closely related to Poiretia and Zornia. All three have legumes with crests or bristles on each pod article and leaves that are usually paripinnate (a few species of Poiretia have imparipinnate leaves). Amicia differs from Poiretia and Zornia in having blunt keel petals, a staminal sheath that is split open above, and anthers that are mostly uniform. A recent attempt to segregate Poiretia and Zornia from Amicia (Ohashi, 1999
) is not supported by this analysis.
Poiretia Vent. is confined to the Neotropics but with most species from Brazil to northern Argentina (Rudd, 1972c
). The genus is similar to Zornia, but differs in its usually twining habit and racemose inflorescences with small, single flower bracts at each node.
Zornia J. F. Gmel. occurs in southeastern United States, the Neotropics with a center of diversity in Brazil, and throughout sub-Saharan Africa (Mohlenbrock, 1961, 1962
). It is marked by medifixed stipules (independently evolved in Aeschynomene sect. Aeschynomene and relatives), leaves with digitately arranged few leaflets, and sessile flowers in axils of large paired bracts.
The Pterocarpus clade
Discolobium Benth. is readily diagnosed by its pod that coils in a forward direction with each of three turns compressed together into a single disc. Only the middle loment is fertile. Its 4 + 1 + 4 + 1 diadelphous staminal column is not unique and is found sporadically among the dalbergioids. Discolobium comprises eight species distributed from northern Argentina to adjacent Brazil and Paraguay (Rudd, 1981a
).
Riedeliella Harms comprises three species endemic to southeastern Brazil and Paraguay (Lima and Studart da Fanseca Vaz, 1984
). Like Inocarpus, Etaballia, and some species of Pictetia, the flowers of Riedeliella are nearly radially symmetric. Lima and Studart da Fanseca Vaz (1984)
propose the close relationship of Etaballia and Riedeliella in the tribe Acosmieae (Yakovlev, 1972
), a group also with essentially radially symmetric flowers, although with free staminal filaments. Riedeliella differs from Etaballia and Inocarpus in having paripinnate leaves and a long exerted style, and in this analysis it is suggested to be not most closely related to Etaballia, but rather to Discolobium.
Brya P. Br. is recorded to have explosive pollen release (León and Alain, 1951
, p. 315, fig. 131), a form of pollen presentation that is unique among dalbergioid legumes. Also, Brya is characterized by its leaves from the long shoots being transformed into spines. Brya is sister to Cranocarpus, as evidenced by the shared occurrence of leaves, stems, inflorescences, and pods bearing capitate glandular trichomes that are microscopically glochidiate, and by periporate pollen (Ferguson and Skvarla, 1981
). Brya includes four species endemic to the Greater Antilles (Ohashi, Polhill, and Schubert, 1981
; Lewis, 1988
).
Cranocarpus Bentham comprises three species endemic to Brazil (Harley, 1978
; Ohashi, Polhill, and Schubert, 1981
). In all respects Cranocarpus is like Brya but the leaves from the long shoots are not transformed into spines. The yellow petals, base chromosome number of x = 10, storied wood structure (Record, 1919
), and simple axillary racemes or solitary flowers of Brya and Cranocarpus are traits strongly suggestive of a relationship with the dalbergioid legumes.
Platymiscium Vogel (Figs. 29–36) comprises 18 neotropical species centered in Mexico and northeastern Brazil. The genus is unique in having opposite leaves with interpetiolar stipules (Lima, 1990
; Klitgaard, 1999a, b
).
Centrolobium Mart. ex Benth. comprises six tropical species from Panama to Colombia, Ecuador, Venezuela, Brazil, and Bolivia (Rudd, 1954
; Lima, 1985
). The genus is well marked by its orange peltate glands covering the leaves and inflorescences, and winged pods in which the seed-bearing portion is covered with spines.
Grazielodendron Lima is a monotypic genus endemic to Brazil (Lima, 1983, 1990
). The laterally compressed pod of Grazielodendron is distinguished by having an additional wing-like extension of the dorsal margin. The winged dorsal margin is markedly delineated from the main winged body of the pod.
Pterocarpus Jacq. (Figs. 37–47) comprises 20 species distributed pantropically (Rojo, 1972
). Of the genera with wide, crimped wing petals (i.e., Paramachaerium, Geoffroea, Pterocarpus, Ramorinoa, Paramachaerium, Tipuana, and Platypodium), Pterocarpus is diagnosed by its pod that is winged from an attenuation of the pod body all around the seed chamber (Polhill, 1981d
; Lima, 1990
). The pods are variable in this genus with some winged and bristly (e.g., P. angolensis), others winged and not bristly (e.g., P. indicus), and rarely not winged and not bristly (i.e., P. amazonum).
Tipuana (Benth.) Benth. is a monotypic genus of subtropical forests in Bolivia and northwestern Argentina (Rudd, 1974
). Of the genera with wide, crimped wing petals (see description of Pterocarpus), Tipuana is diagnosed by its pod that is winged from the style, the seed chambers being proximal to the wing (Lima, 1990
; Polhill, 1981d
).
Platypodium Vogel includes one or two species in Panama, Guatemala, Venezuela, Colombia, Bolivia, Brazil, and Paraguay. Of the genera with wide, crimped wing petals (see description of Pterocarpus), Platypodium is diagnosed by its pod that is winged from the stipe, the seed chambers being distal to the wing (Polhill, 1981d
; Lima, 1990
).
Paramachaerium Ducke includes five species from Panama, Guyana, Peru, and Brazil (Rudd, 1981a, b
; Lima, 1990
). Of the dalbergioid tree genera with laterally broadened and crimped wing petals, Paramachaerium has reddish to violet petals rather than the typical yellow pigment. This genus is unusual in its nectariferous disk surrounding the base of the ovary, a trait independently evolved in certain species of Machaerium and Ormocarpum.
Ramorinoa Speg. is a monotypic genus from west-central Argentina. The genus is very well marked by its leafless pungent branches (Burkart, 1952
; Polhill, 1981d
; Lima, 1990
). As remarked by Burkart (1952)
, the genus is so highly modified vegetatively that morphology provides few clues to its closest relationships.
Inocarpus J. R. & G. Forster is very distinctive in having all five ligulate petals fused at base, and with the ten stamens fused by their filaments to the corolla tube (similar to some genera of Amorpheae). Inocarpus comprises one to three species and is geographically distinctive in being restricted to Malaysia and adjacent Pacific islands (Polhill, 1981d
). The only other dalbergioid genus restricted to Asia is Geissaspis.
Etaballia Benth. is very similar to Inocarpus, except that its leaves are unifoliolate rather than simple, and the staminal filaments are monodelphous with no split along the adaxial side. Etaballia is monotypic and unlike Inocarpus is neotropical, occurring in Guyana, Venezuela, and Brazil (Rudd, 1970b
).
Geoffroea Jacq. comprises two species from Colombia and Venezuela south to Chubut, Argentina, and also on the Galapagos Islands possibly due to cultivation (Ireland and Pennington, 1999
). Of the genera with wide, crimped wing petals (see description of Pterocarpus), Geoffroea is diagnosed by its sessile ovary that develops into a fleshy drupe (Polhill, 1981d
; Lima, 1990
).
Cascaronia Griseb. is not readily diagnosed, but the combination of its leaves and pods with dark pustular glands, pods with strong longitudinal nerves, arborescent habit, inflorescences of axillary racemes, and small yellow petals is unique. Cascaronia is a monotypic genus from northern Argentina and adjacent Paraguay and Bolivia (Polhill, 1981d
).
Fissicalyx Bentham is a monotypic genus from Venezuela and Guyana, and marked by its spathaceous calyx (all five lobes are on the adaxial lip), porate anthers, and pods with a fusiform seed chamber bearing a closely veined membranous wing on both margins (Polhill, 1981d
; Lima, 1990
). There is no morphological evidence to suggest that this genus is closely related to Fiebrigiella, as revealed by DNA sequence analysis.
Fiebrigiella Harms is a monotypic genus from Bolivia and Ecuador (Burkart and Vilchez, 1971
). The pods of Fiebrigiella have prominent continuous parallel venation on the lateral walls, once suggesting an affinity to Chaetocalyx and Nissolia (Rudd, 1981a
), but now considered homologous to such pods of the genera Chapmannia, Stylosanthes, and Arachis.
Chapmannia Torr. & Gray is recently expanded from monotypic (Gunn, Norman, and Lassetter, 1980
) to include seven species of seasonally dry vegetation, two New World (Florida and Mesoamerica), and five Old World (Somalia and the Yemeni island Socotra; Thulin, 2000
). Arthrocarpum Balf. f. (Gillett, 1966
) and Pachecoa Standl. & Steyerm. (Burkart, 1957
) are synonymized. The genus is diagnosed by its dried (herbarium preserved) leaflets with uniformly reddish reticulate tannin deposits on the abaxial surface. Chapmannia is sister to Arachis, and Stylosanthes; the species of these two latter genera do not consistently show the reddish tannin reticulations. Chapmannia, Arachis, and Stylosanthes form a monophyletic group marked in part by their sessile flowers with long hypanthia. Within this group, Chapmannia maintains the plesiomorphic spicate inflorescence, whereas Arachis and Stylosanthes have inflorescences of solitary axillary flowers.
Stylosanthes Swartz and Arachis share the synapomorphy of stipules united to nodal projections, which in turn are superficially continuous with the petiole (a trait known also from Adesmia). Stylosanthes is distinguished from Arachis by having lomented, nongeocarpic pods, which are presumably plesiomorphic, as well as ovaries that are uniformly covered by uniseriate trichomes, an autapomorphy. The 25 species of Stylosanthes are distributed in warm temperate to tropical regions of the world, but with a center of diversity in the neotropics (Mohlenbrock, 1957, 1960, 1963
; Rudd, 1981a
).
Arachis L. is distinguished from Stylosanthes by its flowers with a very long and narrow hypanthium, a gynophore (Moctezuma and Feldman, 1998
) that renders the pods geocarpic, nonlomented glabrous pods, and mostly four leaflets per leaf. The 69 species of Arachis originate in South America from a region including Brazil south to northern Argentina (Krapovickas and Gregory, 1994
).
The Dalbergia clade
Dalbergia L. f. (Figs. 48–58) is diagnosed by small ovate to obovate anthers with short transverse slits at dehiscence. The genus includes over 100 species distributed pantropically, but with centers of diversity in Amazonia and Indo-Asia (Prain, 1904
; Pittier, 1922
; Polhill, 1981d
; Lima, 1990
; de Carvalho, 1997
).
Machaerium Pers. (Figs. 59–69) includes 120 neotropical species, although M. lunatum (L. f.) Ducke also occurs in western Africa. Machaerium is related to Dalbergia (Polhill, 1981d
; Doyle et al., 1997
) and Aeschynomene sect. Ochopodium, as evinced in part by inflorescences of helicoid cymes (but polymorphic in all three taxa). Machaerium differs in its spinescent recurved stipules (on at least the climbing species) and pods that are usually distally winged, or at least have the seed chamber toward the base (Rudd, 1973, 1977, 1986, 1987
; Polhill, 1981d
; de N. Carmo-Bastos, 1987
; Lima, 1990
).
Aeschynomene L. sect. Ochopodium. Aeschynomene sensu lato includes species that do not fit the diagnosis of the other dalbergioid genera. It is for this reason that the genus is treated with two terminal taxa, sects. Ochopodium (with basifixed stipules) and Aeschynomene (with medifixed stipules). Section Ochopodium, according to DNA sequence analysis, is more closely related to Machaerium than to sect. Aeschynomene (e.g., section Ochopodium is represented by Aeschynomene purpusii and A. fasicularis in Fig. 5). Regardless, it is not certain if either of these two sections are monophyletic, a topic that will have to be taken up elsewhere given their large taxonomic size. As such, sect. Ochopodium includes 101 species distributed pantropically (Rudd, 1955, 1967, 1975a
).
Aeschynomene sect. Aeschynomene is diagnosed by medifixed stipules, which are also characteristic of the closely related Smithia and Geissaspis. Thus, this taxon (represented by Aeschynomene americana, A. indica, A. pfundii, A. rudis, and A. virginica in Figs. 2 and 5), potentially lacking any obvious morphological apomorphy, could be paraphyletic with respect to at least some of the genera listed immediately below. It is beyond the scope of this analysis to address this potential problem. As such, sect. Aeschynomene comprises 50 species with a pantropical distribution (Léonard, 1954
; Rudd, 1955, 1959, 1972a
; Verdcourt, 1971
; Fernandes, 1996
).
Soemmeringia Mart. is characterized by a scarious standard petal that persists with the mature pod, which is independently evolved in some species of Ormocarpum. Soemmeringia is a monotypic, neotropical genus from Brazil, Bolivia, and Venezuela (Rudd, 1981a
). Soemmeringia, along with Cyclocarpa, Kotschya, Smithia, Geissaspis, Bryaspis, and Humularia (below), are all closely related to sect. Aeschynomene because of their paripinnate leaves, usually alternate leaflets, and bilabiate calyces (Rudd, 1981a
).
Cyclocarpa Afz. ex Bak. is diagnosed by pods that have one lateral spiral, the pod articles of which disarticulate from a persistent placental margin or replum. This monotypic genus is locally common across tropical Africa, and in southeast Asia (Laos and Borneo) and northern Australia (Hepper, 1958
).
Kotschya Endl. and Smithia (below) are characterized by an inflorescence of a dense strobilate helicoid cyme, a pod enclosed by the calyx and in which the articles are folded against each other. Kotschya differs in having alternate leaflets that each bear 2–7 basal nerves, as well as basifixed stipules. Kotschya comprises 31 species restricted to tropical Africa and Madagascar (Gillett, Polhill, and Verdcourt, 1971
; Verdcourt, 1974
; Rudd, 1981a
).
Smithia Ait. differs from Kotschya by its medifixed stipules and opposite leaflets each bearing one main nerve. Smithia comprises 30 species mainly in Asia and Madagascar (Gillett, Polhill, and Verdcourt, 1971
; Verdcourt, 1974
; Rudd, 1981a
).
Geissaspis Wight & Arn. together with Bryaspis and Humularia (below) are characterized by large inflorescence bracts that completely envelop the subtending flower and fruit (independently evolved in Zornia). Geissaspis and Bryaspis differ by ebracteolate flowers, and Geissaspis differs from Bryaspis by its medifixed stipules. Geissaspis comprises three species confined to tropical and subtropical central and southeast Asia, but not crossing Wallace's line (Gledhill, 1968
; Rudd, 1981a
)
Bryaspis Duvign. includes two species from tropical west Africa (Gledhill, 1968
; Hepper, 1958
; Gillett, Polhill, and Verdcourt, 1971
; Rudd, 1981a
). Unlike Geissaspis, the inflorescence bracts of Bryaspis are markedly imbricate.
Humularia Duvign. differs from Geissaspis and Bryaspis by emarginate inflorescence bracts and panduriform standard petals. Humularia comprises 40 species confined to central Africa (Gledhill, 1968
; Gillett, Polhill, and Verdcourt, 1971
; Verdcourt, 1974
; Rudd, 1981a
).
Weberbauerella Ulbrich is diagnosed by the combination of its herbaceous habit, pustular glands densely covering the stems, leaves, and inflorescences (including petals), and leaves with well over 40 leaflets. Similar pustular glands on the petals are known from Poiretia, but this genus is marked by leaves with four leaflets, and a sometimes climbing habit. Weberbauerella contains two species confined to sand in southern coastal Peru (Ferreyra, 1951
; Rudd, 1981a
).
Pictetia DC. is characterized by spiny stipules, short shoots bearing distichously arranged stipules (shared with Ormocarpum, Ormocarpopsis, and Peltiera), coriaceous leaflets that in all but two species have spinescent mucros, and pods with two-ribbed placental margins. Pictetia includes eight species confined to Cuba, Hispaniola, Puerto Rico, and the Virgin Islands excluding St. Croix (Beyra-M. and Lavin, 1999
).
Diphysa Jacq. has been characterized by its mature pods that have an exocarp distinctly inflated and separated from the mesocarp. However, Diphysa ormocarpoides and D. spinosa have laterally flattened lomented pods very similar to species of Ormocarpum and Pictetia (Antonio and Sousa, 1991
). The monophyly of this genus is strongly supported, however, by phylogenetic analysis of molecular data (see also Beyra-M. and Lavin, 1999
; Lavin et al., 2000
). The genus includes about ten species centered in Mexico and Central America (M. Lavin, unpublished data).
Ormocarpum P. Beauv. is diagnosed by most species forming a cylindrical nectary disk surrounding the base of the ovary (M. Thulin and M. Lavin, unpublished data). This trait otherwise is known in a few species of Machaerium and Paramachaerium. This genus of 20 species is primarily African. Three species occur on the southern Arabian Peninsula in Yemen (including Socotra) and Oman, and one to two species occur in tropical Asia and Australia (Gillett, 1966
; Rudd, 1981a
; Thulin, 1990
). According to ITS/ 5.8S sequence data (see also Lavin et al., 2000
), Ormocarpum comprises two lineages (one with and one without the intrastaminal disk) that are collectively paraphyletic with respect to Ormocarpopsis (and Peltiera). This issue is being addressed in a separate study (M. Thulin and M. Lavin, unpublished data).
Ormocarpopsis R. Viguier has short shoots with persistent distichously arranged stipules shared with Ormocarpum, Peltiera, and Pictetia. In this context, its non-lomented pod with a smooth exocarp (no evidence of prominent parallel nervation on the pod valves) and tannin patches on the abaxial surface of dried leaflets are diagnostic. Ormocarpopsis comprises six species endemic to Madagascar (Labat and Du Puy, 1996
).
Peltiera Labat & Du Puy includes two endemic Madagascan species that are sister to Ormocarpopsis (Labat and Du Puy, 1997
). These two genera share a distinctive tannin patterning on the abaxial surface of herbarium-dried leaflets where tannin deposits are concentrated along the midrib. Like Ormocarpopsis, the flowers of Peltiera lack a nectary disk (M. Thulin and M. Lavin, unpublished data), and the pods, though lomented and with all but one loment aborting, contain spherical seeds. The pod valves in the seed-bearing article are dehiscent. Unfortunately, both species of Peltiera are probably extinct due to the clearing of forests from which they were known.
|
FOOTNOTES |
|---|
2 Author for reprint requests (e-mail: mlavin{at}montana.edu
)
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITEDAPPENDIXAPPENDIX |
|---|
Bailey, C. D., J. J. Doyle, T. Kajita, T. Nemoto, and H. Ohashi. 1997 The chloroplast rpl2 intron and ORF184 as phylogenetic markers in the legume tribe Desmodieae. Systematic Botany 22: 133–138
Baretta-Kuipers, T. 1981 Wood anatomy of Leguminosae: its relevance to taxonomy. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 2, 677–705. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Barneby, R. C. 1977 Daleae imagines. Memoirs of the New York Botanical Garden 27: 1–891
Bateman, R. M., and N. J. Simpson. 1998 Comparing phylogenetic signals from reproductive and vegetative organs. In S. J. Owens and P. J. Rudall [eds.], Reproductive biology in systematics, conservation and economic botany, 231–253. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Bentham, G. 1860 A synopsis of the Dalbergieae, a tribe of the Leguminosae. Journal of the Proceedings of The Linnean Society IV(Supplement): 1–134
Beyra-M., A., and M. Lavin. 1999 Monograph of Pictetia (Leguminosae—Papilionoideae) and review of the Aeschynomeneae. Systematic Botany Monographs 56: 1–93
Bininda-Emonds, O. R. P., H. N. Bryant, and A. P. Russell. 1998 Supraspecific taxa as terminals in cladistic analysis: implicit assumptions of monophyly and a comparison of methods. Biological Journal of the Linnean Society 64: 101–133
Brizicky, G. K. 1960 A new species of Paramachaerium from Panama. Tropical Woods 112: 58–64
Burkart, A. 1949 Contribución al estudio del género Adesmia (Leguminosae). Lilloa 15: 1–17
———. 1952 Las Leguminosas Argentinas, 2nd ed. ACME Agency, Buenuos Aires, Argentina
———. 1954 Contribución al estudio del género Adesmia (Leguminosae), II. Darwiniana 10: 465–546
———. 1957 El género Pachecoa (Leguminosae). Darwiniana 11: 261– 268
———. 1960 Contribución al estudio del género Adesmia (Leguminosae), III. Darwiniana 12: 81–136
———. 1962 Contribución al estudio del género Adesmia (Leguminosae), IV. Darwiniana 12: 309–364
———. 1964 Contribución al estudio del género Adesmia (Leguminosae), V. Darwiniana 13: 9–66
———. 1966 Contribución al estudio del género Adesmia (Leguminosae), VI. Darwiniana 14: 195–248
———. 1967 Sinopsis del género sudamericano de Leguminosas Adesmia DC. Darwiniana 14: 463–568
———, and O. Vilchez. 1971 Valoración e ilustración del género Fiebrigiella Harms (Leguminosae-Hedysareae). Darwiniana 16: 659–662
Chappill, J. 1995 Cladistic analysis of the Leguminosae. In M. D. Crisp and J. J. Doyle [eds.], Advances in legume systematics, part 7, phylogeny, 1–9. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Corby, H. D. L. 1981 The systematic value of leguminous root nodules. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 2, 657–669. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1988 Types of rhizobial nodule and their distribution among the Leguminosae. Kirkia 13: 53–123
Cozzo, D. 1949 Estudio anatomico sobre la posicion sistematica de algunos generos Argentinos de Leguminosas Papilionoideas. Lilloa 16: 97–124
———. 1950 Anatomia del leño secundario de las Leguminosas Papilionoideas Argentinas silvestres y cultivadas. Revista del Instituto Nacional de Investigacion de las Ciencias Naturales "Bernadino Rivadavia". Ciencias Botanicas I(7): 223–361
Cumbie, B. G. 1960 Anatomical studies in the Leguminosae. Tropical Woods 113: 1–47
Cunningham, C. W. 1997 Is congruence between data partitions a reliable predictor of phylogenetic accuracy? Empirically testing an interactive procedure for choosing among phylogenetic methods. Systematic Biology 46: 464–478[CrossRef][Web of Science][Medline]
de Candolle, A. P. 1825 Mémoires sur la famille de Légumineuses. Paris, France
de Carvalho, A. M. 1997 A synopsis of the genus Dalbergia (Fabaceae: Dalbergieae) in Brazil. Brittonia 49: 87–109[CrossRef][Web of Science]
de N. Carmo-Bastos, M. 1987 Contribuição ao estudo sistemático de algumas espécies do gênero Machaerium Persoon (Leguminosae—Papilionoideae) ocorrentes na Amazônia Brasileira. Boletim do Museu Paraense Emílio Goeldi, Série Botânica. 3: 183–279
Delgado-Salinas, A., T. Turley, A. Richman, and M. Lavin. 1999 Phylogenetic analysis of the cultivated and wild species of Phaseolus (Fabaceae). Systematic Botany 23: 438–460
de Queiroz, K., and J. Gauthier. 1994 Toward a phylogenetic system of biological nomenclature. Trends in Ecology and Evolution 9: 27–31
Détienne, P., and P. Jacquet. 1983 Atlas d'identification des bois de l'Amazonie et des règions voisines. Centre Technique Forestier Tropical, Nogent-sur-Marne, France
Doyle, J. J., J. L. Doyle, J. A. Ballenger, E. E. Dickson, T. Kajita, and H. Ohashi. 1997 A phylogeny of the chloroplast gene rbcL in the Leguminosae: Taxonomic correlations and insights into the evolution of nodulation. American Journal of Botany 84: 541–554[Abstract]
Evans, S. V., L. E. Fellows, and E. A. Bell. 1985 Distribution and systematic significance of basic nonprotein amino acids and amines in the Tephrosieae. Biochemical Systematics and Ecology 13: 271–302
Faria, S. M. de, and H. C. de Lima. 1998 Additional studies of the nodulation status of legume species in Brazil. Plant and Soil 200: 185–192[CrossRef][Web of Science]
———, H. C. de Lima, A. M. Carvalho, V. F. Concalves, and J. I. Sprent. 1994 Occurrence of nodulation in legume species from Bahia, Minas Gerais, and Espirito Santo states of Brazil. In J. I. Sprent and D. McKey [eds.], Advances in legume systematics, part 5, the nitrogen factor, 17–23. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Felsenstein, J. 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 38: 783–791
Ferguson, I. K., and J. J. Skvarla. 1981 The pollen morphology of the subfamily Papilionoideae (Leguminosae). In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 2, 859–896. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Fernandes, A. 1996 O Taxon Aeschynomene no Brasil. Fortaleza: Edicoes UFC
Ferreyra, R. 1951 Una nueva Leguminosae del Peru. Publicaciones del Museo de Historia Natural "Javier Prado," Serie B, Botánica 3: 1–5
Gasson, P. E. 1994 Wood anatomy of the tribe Sophoreae and related Caesalpinioideae and Papilionoideae. In I. K. Ferguson and S. C. Tucker [eds.], Advances in legume systematics, part 6, 165–203. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1999 Wood anatomy of the tribe Dipterygeae with comments on related Papilionoid and Caesalpinioid Leguminosae. IAWA Journal 20: 361–375
Geesink, R. 1981 Tephrosieae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 1, 245–260. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1984 Scala Millettiearum, a survey of the genera of the tribe Millettieae (Legum.—Pap.) with methodological considerations. E. J. Brill/ Leiden University Press, Leiden, The Netherlands
Gillett, J. B. 1966 The species of Ormocarpum Beauv. and Arthrocarpum Balf. f. (Leguminosae) in South-Western Asia and Africa (excluding Madagascar). Kew Bulletin 20: 323–355[CrossRef]
———, R. M. Polhill, and B. Verdcourt. 1971 Leguminosae. In E. Milne-Redhead and R. M. Polhill [eds.], Flora of Tropical East Africa. Crown Agents, London, UK
Gledhill, D. 1968 The Geissaspis, Bryaspis, Humularia complex. Boletim da Sociedade Broteriana, serie 2: 305–319
Goldblatt, P. 1981 Cytology and the phylogeny of the Leguminosae. In R. M. Polhill and P. H. Raven [eds.], Advances in legumes systematics, part 2, 427–463. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Greinwald, R., P. Bachmann, G. Lewis, L. Witte, and F.-C. Czygan. 1995 Alkaloids of the genus Poecilanthe (Leguminosae: Papilionoideae). Biochemical Systematics and Ecology 23: 547–553[CrossRef]
Gualtieri, G., and T. Bisseling. 2000 The evolution of nodulation. Plant Molecular Biology 42: 181–194[CrossRef][Web of Science][Medline]
Guinet, Ph., and I. K. Ferguson. 1989 Structure, Evolution, and Biology of Pollen in Leguminosae. In C. H. Stirton and J. L. Zarucchi [eds.], Advances in legume biology. Monographs in Systematic Botany from the Missouri Botanical Garden 29: 77–103
Gunn, C. R., E. M. Norman, and J. S. Lassetter. 1980 Chapmannia floridana Torrey & Gray (Fabaceae). Brittonia 32: 178–185[CrossRef][Web of Science]
Harley, R. M. 1978 A study of Cranocarpus in Brazil. Bradea, Bolitim do Herbarium Bradeanum 2: 265–272
Harrier, L. A. 1995 Non-nodulating African species of Acacia. Ph.D. dissertation, University of Dundee, Dundee, UK
———, P. W. Whitty, J. M. Sutherland, and J. I. Sprent. 1997 Phenetic investigation of non-nodulating African species of Acacia (Leguminosae) using morphological and molecular markers. Plant Systematics and Evolution 205, 27–51
Hepper, F. N. 1958 Papilionaceae. In R. W. J. Keay [ed.], Flora of West Tropical Africa, 2nd ed. Crown Agents, London, UK
Herendeen, P. S. 1995 Phylogenetic relationships of the tribe Swartzieae. In M. Crisp and J. J. Doyle [eds.], Advances in legume systematics, part 7, phylogeny, 123–132. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Hillis, D. 1998 Taxonomic sampling, phylogenetic accuracy, and investigator bias. Systematic Biology 47: 3–8
Hu, J.-M., M. Lavin, M. Wojciechowski, and M. J. Sanderson. 2000 Phylogenetic systematics of the tribe Millettieae (Leguminosae) based on chloroplast trnK/matK sequences, and its implications for evolutionary patterns in Papilionoideae. American Journal of Botany 87: 418–430
Huelsenbeck, J. P., J. J. Bull, and C. W. Cunningham. 1996 Combining data in phylogenetic analysis. Trends in Ecology and Evolution 11: 152– 158[CrossRef]
Hutchinson, J. 1964 The genera of flowering plants, vol. 1. Oxford University Press, Oxford, UK
Ireland, H., and R. T. Pennington. 1999 A revision of Geoffroea (Leguminosae—Papilionoideae). Edinburgh Journal of Botany 56: 329–347
James, E. K., J. I. Sprent, J. M. Sutherland, S. G. McInroy, and F. R. Minchin. 1992 The structure of nitrogen fixing root nodules on the aquatic mimosoid legume Neptunia plena. Annals of Botany 69: 173– 180
Judd, W. S., R. W. Sanders, and M. J. Donoghue. 1994 Angiosperm family pairs: preliminary phylogenetic analyses. Harvard Papers in Botany 5: 1–51
Käss, E., and M. Wink. 1995 Molecular phylogeny of the Papilionoideae (Family Leguminosae): rbcL gene sequences versus chemical taxonomy. Botanica Acta 108: 149–162
———, and ———. 1997 Phylogenetic relationships in the Papilionoideae (Family Leguminosae) based on nucleotide sequences of cpDNA (rbcL) and ncDNA (ITS 1 and 2). Molecular Phylogenetics and Evolution 8: 65–88[CrossRef][Web of Science][Medline]
Klitgaard, B. B. 1999a Floral ontogeny in tribe Dalbergieae (Leguminosae: Papilionoideae): Dalbergia brasiliensis, Machaerium villosum sens lat., Platymiscium floribundum, and Pterocarpus rotundifolius. Plant Systematics and Evolution 219: 1–25[CrossRef][Web of Science]
———. 1999b New species and nomenclatural changes in Neotropical Platymiscium (Leguminosae: Papilionoideae: Dalbergieae). Kew Bulletin 54: 967–973[CrossRef]
Krapovickas, A., and W. C. Gregory. 1994 Taxonomía del género Arachis (Leguminosae). Bonplandia 8: 1–186
Labat J.-N., and D. J. Du Puy. 1996 Two species of Ormocarpopsis R. Viguier and a new combination in Ormocarpum P. Beauvois (Leguminosae—Papilionoideae) from Madagascar. Novon 6: 54–58[CrossRef]
———, and ———. 1997 A revision of Peltiera, a new, poorly known and probably extinct genus of Leguminosae (Papilionoideae—Aeschynomeneae) from Madagascar. Adansonia, série 3, 19: 85–91
Lavin, M. 1987 A cladistic analysis of the tribe Robinieae (Papilionoideae: Leguminosae). In C. H. Stirton [ed.], Advances in legumes systematics, part 3, 31–64. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1993 Biogeography and systematics of Poitea (Leguminosae). Systematic Botany Monographs 37: 1–87
———, E. Eshbaugh, J.-M. Hu, S. Mathews, and R. A. Sharrock. 1998 Monophyletic subgroups of the tribe Millettieae (Leguminosae) as revealed by phytochrome nucleotide sequence data. American Journal of Botany 85: 412–433[Abstract]
———, and M. Sousa. 1995 Phylogenetic systematics and biogeography of the tribe Robinieae (Leguminosae). Systematic Botany Monographs 45: 1–165
———, M. Thulin, J.-N. Labat, and T. Pennington. 2000 Africa, the odd man out: molecular biogeography of dalbergioid legumes suggests otherwise. Systematic Botany 24: in press
León, H., and H. Alain. 1951 Leguminosas, Flore de Cuba, vol. 2, Contribuciones Ocasionales del Museo de la Historia Natural del Colegio de La Salle 10: 224–367
Léonard, J. 1954 Aeschynomene. Bulletin du Jardin Botanique de l'état Bruxelles 24: 63–84[CrossRef]
Lewis, G. 1988 Four little-known species of Leguminosae from Cuba. Willdenowia 18: 223–229
Lima, H. C. de. 1982a Considerações taxonômicas sobre o gênero Hymenolobium Bentham (Leguminosae—Faboideae). Acta Amazonica 12: 41–48
———. 1982b Revisão taxonômica do gênero Vatairea Aublet (Leguminosae—Faboideae). Arquivos do Jardim Botânico do Rio de Janeiro XXVI: 173–214
———. 1983 Novos taxa de Leguminosae Papilionoideae (tribo Dalbergieae) do Brasil. Bradea, Bolitim do Herbarium Bradeanum 3: 399–405
———. 1985 Centrolobium Martius ex Bentham (Leguminosae—Papilionoideae) estudo taxonômico das espécies Brasileiras extra-Amazônicas. Arquivos do Jardim Botânico do Rio de Janeiro XXVII: 177–191
———. 1990 Tribo Dalbergieae (Leguminosae Papilionoideae)—morfologia do frutos, sementes e plântulas e sua aplicação na sistemática. Arquivos do Jardim Botânico do Rio de Janeiro 30: 1–42
———, and A. M. Studart da Fanseca Vaz. 1984 Revisão taxonômica do género Riedeliella Harms (Leguminosae—Faboideae). Rodriguesia, Rio De Janeiro 36: 9–16
Miles, A. 1978 Photomicrographs of world woods. Her Majesty's Stationery Office, London, UK
Maddison, W. P., and D. R. Maddison. 1999 MacClade: analysis of phylogeny and character evolution. Version 3.08a. Sinauer, Sunderland, Massachusetts, USA
Moctezuma, E., and L. J. Feldman. 1998 Growth rates and auxin effects in graviresponding gynophores of the peanut, Arachis hypogaea (Fabaceae). American Journal of Botany 85: 1369–1376
Mohlenbrock, R. H. 1957 A revision of the genus Stylosanthes. Annals of the Missouri Botanical Garden 44: 299–355[CrossRef]
———. 1960 Recent studies in the Leguminosae genus Stylosanthes. Rhodora 62: 340–346
———. 1961 A monograph of the Leguminous genus Zornia. Webbia 16: 1–141
———. 1962 Additional collections of the Leguminous genus Zornia. Webbia 16: 649–655
———. 1963 Further considerations in Stylosanthes (Leguminosae). Rhodora 65: 245–258
Molouba, F., J. Lorquin, A. Willems, B. Hoste, E. Giraud, B. Dreyfus, M. Gillis, P. de Lajudie, C. Masson-Boivin. 1999 Photosynthetic bradyrhizobia from Aeschynomene spp. are specific to stem nodulating species and form a separate 16S ribosomal DNA restriction fragment length polymorphism group. Applied and Environmental Microbiology 65: 3084–3094
Nixon, K. C., and J. I Davis. 1991 Polymorphic taxa, missing values and cladistic analysis. Cladistics 7: 233–241[CrossRef][Web of Science]
Ohashi, H. 1999 The genera, tribes, and subfamilies of Japanese Leguminosae. The Science reports of the Tohoku University, 4th series Biology 40: 187–268
———, R. M. Polhill, and B. G. Schubert. 1981 Desmodieae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 1, 292–300. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Pennington, R. T. 1996 Molecular and morphological data provide phylogenetic resolution at different hierarchical levels in Andira. Systematic Biology 45: 496–515[CrossRef]
———, G. Aymard, and N. Cuello. 1997 A new species of Andira (Leguminosae, Papilionoideae) from the Venezuelan Guyana. Novon 7: 72– 74[CrossRef][Web of Science]
———, M. Lavin, H. Ireland, B. Klitgaard, and J. Preston. In press Phylogenetic relationships of primitive papilionoid legumes based upon sequences of the chloroplast intron trnL. Systematic Botany.
Pittier, H. 1922 On the species of Dalbergia of Mexico and Central America. J. Washington Academy of Science 12: 54–64
Polhill, R. M. 1971 Some observations on generic limits in Dalbergieae- Lonchocarpineae Benth. (Leguminosae). Kew Bulletin 25: 259–273[CrossRef]
———. 1981a Papilionoideae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 1, 191–208. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1981b Sophoreae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 1, 213–230. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1981c Dipterygeae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 1, 231–232. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1981d Dalbergieae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 1, 233–242. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1981e Amorpheae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 1, 244–246. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1981f Adesmieae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 1, 355–356. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1994 Classification of the Leguminosae. In F. A. Bisby, J. Buckingham, and J. B. Harborne [eds.], Phytochemical dictionary of the Leguminosae, vol. 1, XXXV–XLVIII. Chapman and Hall, London, UK
Prain, D. 1904 The species of Dalbergia of South-eastern Asia. Annals of the Royal Botanical Gardens, Calcutta 10: 1–114, 91 pl
Rambaut, A. 1996 Se-Al, sequence alignment editor version 1.0, alpha 1. University of Oxford, Oxford, UK
Record, S. J. 1919 Storied or tier-like structure of certain dicot wood. Bulletin of the Torrey Botanical Club 46: 253–273[CrossRef]
Roig, F. A. 1986 The wood of Adesmia horrida and its modifications by climatic conditions. IAWA Bulletin 7: 129–135
Rojo, J. P. 1972 Pterocarpus (Leguminosae—Papilionaceae) revised for the world. Verlag von J. Cramer, Lehre, Germany
Rudd, V. E. 1954 Centrolobium (Leguminosae). Validation of a specific name and a brief review of the genus. Journal of the Washington Academy of Science 44: 284–288
———. 1955 The American species of Aeschynomene. Contributions of the United States National Herbarium 32: 1–172
———. 1956 A revision of the genus Nissolia. Contributions of the United States National Herbarium 32: 173–206
———. 1958 A revision of the genus Chaetocalyx. Contributions of the United States National Herbarium 32: 207–243
———. 1959 The genus Aeschynomene in Malaysia (Leguminosae—Papilionatae). Reinwardtia 5: 23–36
———. 1967 Supplementary studies in Aeschynomene, II: Series Pleuronerviae. Phytologia 15: 114–119
———. 1970a Revival of Nissolia microptera (Leguminosae). Phytologia 20: 324
———. 1970b Etaballia dubia (Leguminosae), a new combination. Phytologia 20: 426–428
———. 1972a Reduction of Balisaea to Aeschynomene (Leguminosae). Phytologia 23: 321
———. 1972b Supplementary studies in Chaetocalyx I. (Leguminosae). Including a new species from Brazil. Phytologia 24: 295–297
———. 1972c A new variety of Poiretia latifolia and a brief resume of the genus Poiretia Vent. (Leguminosae). Phytologia 23: 141–148
———. 1973 New taxa and combinations in Machaerium (Leguminosae). III. Phytologia 25: 398–403
———. 1974 A resume of the genus Tipuana (Leguminosae). Phytologia 28: 475–478
———. 1975a Supplementary studies in Aeschynomene III: Series Scopariae in Mexico and Central America. Phytologia 31: 431–434
———. 1975b Nissolia chiapensis, a new species of Leguminosae from Mexico. Phytologia 31: 427–430
———. 1977 The genus Machaerium (Leguminosae) in Mexico. Boletín de la Sociedad Botanica de Mexico 37: 119–146
———. 1981a Aeschynomeneae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 1, 347–354. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1981b Two new species of Paramachaerium (Leguminosae) and a brief resume of the genus. Brittonia 33: 435–440[CrossRef][Web of Science]
———. 1986 A new species of Machaerium (Leguminosae) from Nicaragua. Phytologia 60: 93–94
———. 1987 Studies in Machaerium (Leguminosae) VII. Section II. Lineata. Part I. Species with wingless fruit. Phytologia 64: 1–12
———. 1996 Chaetocalyx longiloba (Fabaceae, Papilionoideae), a new species from Peru. Novon 6: 119
Sanderson, M. J. 1995 Objections to bootstrapping phylogenies: a critique. Systematic Biology 44: 299–320[CrossRef]
———, and J. J. Doyle. 1993 Phylogenetic relationships in North American Astragalus (Fabaceae) based on chloroplast DNA restriction site variation. Systematic Botany 18: 395–408[CrossRef][Web of Science]
———, and M. F. Wojciechowski. 1996 Diversification rates in a temperate legume clade: are there "so many species of Astragalus (Fabaceae)?" American Journal of Botany 83: 1488–1502[CrossRef][Web of Science]
Schweingruber, F. H. 1990 Anatomy of European woods. Paul Haupt, Bern and Stuttgart Publishers, Stuttgard, Germany
Soltis, D. E., P. S. Soltis, D. R. Morgan, S. M. Swensen, B. C. Mullen, J. M. Dowd, and P. G. Martin. 1995 Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences, USA 92: 2647–2651
Sousa, M., and M. P. de Sousa. 1981 New World Lonchocarpinae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, part 1, 261–281. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Sprent, J. I. 1994 Evolution and diversity in the legume-rhizobium symbiosis: chaos theory? Plant and Soil 161: 1–10[CrossRef][Web of Science]
———, and P. Sprent. 1990 Nitrogen fixing organisms. Chapman and Hall, London, UK
———, J. M. Sutherland, and S. M. de Faria. 1989 Structure and function of root nodules from woody legumes. In C. H. Stirton and J. L. Zarucchi [eds.], Advances in legume biology. Monographs in Systematic Botany from the Missouri Botanical Garden 29: 559–578
Swofford, D. L. 2000 PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b4a. Sinauer, Sunderland, Massachusetts, USA
Taberlet, P., L. Gielly, G. Pautou, and J. Bouvet. 1991 Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17: 1105–1109[CrossRef][Web of Science][Medline]
Thulin, M. 1990 Two new species of Ormocarpum (Leguminosae) from Somalia. Nordic Journal of Botany 10: 433–436
———. 2000 Chapmannia (Leguminosae—Stylosanthinae) extended. Nordic Journal of Botany 19: 597–607[Web of Science]
Tucker, S. C., and A. W. Douglas. 1994 Ontogenetic evidence and phylogenetic relationships among basal taxa of legumes. In I. K. Ferguson and S. Tucker [eds.], Advances in legume systematics, part 6, structural botany, 11–32. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Ulibarri, E. A. 1978 Novedades en Adesmia (Leguminosae). Hickenia 1: 121–124
———. 1980 Notas sobre Adesmia I (Leguminosae—Papilionoideae). Darwiniana 22: 493–498
———. 1982a Notas sobre Adesmia DC. II (Leguminosae—Papilionoideae). Darwiniana 24: 267–281
———. 1982b Nueva especie de Adesmia DC. (Leguminosae—Papilionoideae) de Chile. Hickenia 1: 277–290
———. 1984 Notas sobre Adesmia DC. III (Leguminosae—Papilionoideae). Darwiniana 25: 355–360
———. 1987 Las especies de Adesmia de la serie Microphyllae (Leguminosae—Papilionoideae). Darwiniana 27: 315–388
———. 1990 Notas sobre Adesmia IV. (Leguminosae—Papilionoideae). Darwiniana 30: 291–292
Verdcourt, B. 1971 Aeschynomene. In J. B. Gillett, R. M. Polhill, and B. Verdcourt [eds.], Flora of Tropical East Africa, Leguminosae, Papilionoideae, 364–406. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
———. 1974 Summary of the Leguminosae-Papilionoideae-Hedysareae (sensu lato) of Flora Zambesiaca. Kirkia 9: 359–556
Weins, J. J. 1995 Polymorphic characters in phylogenetic systematics. Systematic Biology 44: 482–500[CrossRef][Web of Science]
———, and M. R. Servedio. 1997 Accuracy of phylogenetic analysis including and excluding polymorphic characters. Systematic Biology 46: 332–345[CrossRef]
Wheeler, E. A., P. Baas, and P. E. Gasson. 1989 IAWA list of microscopic features for hardwood identification. IAWA Journal 10: 219–332
Whiting, M. F., J. C. Carpenter, Q. D. Wheeler, and W. C. Wheeler. 1997 The strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 46: 1–68[CrossRef][Web of Science][Medline]
Wojciechowski, M. F., M. J. Sanderson, B. G. Baldwin, and M. J. Donoghue. 1993 Monophyly of anueploid Astragalus (Fabaceae): evidence from nuclear ribosomal DNA-ITS sequences. American Journal of Botany 80: 711–722[CrossRef][Web of Science]
———, ———, and J.-M. Hu. 1999 Evidence on the monophyly of Astragalus (Fabaceae) and its major subgroups based on nuclear ribosomal DNA ITS and chloroplast DNA trnL intron data. Systematic Botany 24: 409–437
Yakovlev, G. P. 1972 A contribution to the system of the order Fabales Nakai (Leguminales Jones). Botanical Journal 57: 585–594 (in Russian—English translation at Royal Botanic Gardens, Kew, Richmond, Surrey, UK)
This article has been cited by other articles:
|
|
 |
|
  B. D. Schrire, M. Lavin, N. P. Barker, and F. Forest Phylogeny of the tribe Indigofereae (Leguminosae-Papilionoideae): Geographically structured more in succulent-rich and temperate settings than in grass-rich environments Am. J. Botany, April 1, 2009; 96(4): 816 - 852. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Saslis-Lagoudakis, M. W. Chase, D. N. Robinson, S. J. Russell, and B. B. Klitgaard Phylogenetics of neotropical Platymiscium (Leguminosae: Dalbergieae): systematics, divergence times, and biogeography inferred from nuclear ribosomal and plastid DNA sequence data Am. J. Botany, October 1, 2008; 95(10): 1270 - 1286. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. A. Scherson, R. Vidal, and M. J. Sanderson Phylogeny, biogeography, and rates of diversification of New World Astragalus (Leguminosae) with an emphasis on South American radiations Am. J. Botany, August 1, 2008; 95(8): 1030 - 1039. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. I. Sprent 60Ma of legume nodulation. What's new? What's changing? J. Exp. Bot., March 1, 2008; 59(5): 1081 - 1084. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. I. Sprent and E. K. James Legume Evolution: Where Do Nodules and Mycorrhizas Fit In? Plant Physiology, June 1, 2007; 144(2): 575 - 581. [Full Text] [PDF]
|
|
|
|
 |
|
 M. M. McMahon and M. J. Sanderson Phylogenetic Supermatrix Analysis of GenBank Sequences from 2228 Papilionoid Legumes Syst Biol, October 1, 2006; 55(5): 818 - 836. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. E Hughes, R. J Eastwood, and C Donovan Bailey From famine to feast? Selecting nuclear DNA sequence loci for plant species-level phylogeny reconstruction Phil Trans R Soc B, January 29, 2006; 361(1465): 211 - 225. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. M. Haston, G. P. Lewis, and J. A. Hawkins A phylogenetic reappraisal of the Peltophorum group (Caesalpinieae: Leguminosae) based on the chloroplast trnL-F, rbcL and rps16 sequence data Am. J. Botany, August 1, 2005; 92(8): 1359 - 1371. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Lavin, P. S. Herendeen, and M. F. Wojciechowski Evolutionary Rates Analysis of Leguminosae Implicates a Rapid Diversification of Lineages during the Tertiary Syst Biol, August 1, 2005; 54(4): 575 - 594. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. F. Wojciechowski, M. Lavin, and M. J. Sanderson A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family Am. J. Botany, November 1, 2004; 91(11): 1846 - 1862. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. McMahon and L. Hufford Phylogeny of Amorpheae (Fabaceae: Papilionoideae) Am. J. Botany, August 1, 2004; 91(8): 1219 - 1230. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. J. Doyle and M. A. Luckow The Rest of the Iceberg. Legume Diversity and Evolution in a Phylogenetic Context Plant Physiology, March 1, 2003; 131(3): 900 - 910. [Full Text] [PDF]
|
|
|
|
|
|
H. L. Citerne, D. Luo, R. T. Pennington, E. Coen, and Q. C.B. Cronk A Phylogenomic Investigation of CYCLOIDEA-Like TCP Genes in the Leguminosae Plant Physiology, March 1, 2003; 131(3): 1042 - 1053. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
